Botrychium hesperium Barneby (western moonwort) A Technical Conservation Assessment

Prepared for the USDA Forest Service, Rocky Mountain Region, Species Conservation Project

April 12, 2004

David G. Anderson and Dan Cariveau Colorado Natural Heritage Program Colorado State University Fort Collins, CO 80523

Peer Review Administered by Center for Plant Conservation Anderson, D.G. and D. Cariveau (2004, April 12). Botrychium hesperium Barneby (western moonwort): a technical conservation assessment. [Online]. USDA Forest Service, Rocky Mountain Region. Available: http:// www.fs.fed.us/r2/projects/scp/assessments/botrychiumhesperium.pdf [date of access].

ACKNOWLEDGEMENTS

This research was greatly facilitated by the helpfulness and generosity of many experts, particularly Reed Crook, Don Farrar, Warren Hauk, Cindy Johnson-Groh, Peter Root, Dave Steinmann, Florence Wagner, and Loraine Yeatts. Their interest in the project and their time spent answering our questions were extremely valuable. Dr. Kathleen Ahlenslager also provided valuable assistance and literature. The Natural Heritage Program/Natural Heritage Inventory/Natural Diversity Database Botanists we consulted (Craig Freeman, Joyce Gould, Bonnie Heidel, Dave Ode, Gerry Steinauer) were also extremely helpful. Greg Hayward, Gary Patton, Jim Maxwell, Andy Kratz, Beth Burkhart, and Joy Bartlett assisted with questions and project management. Jane Nusbaum, Carmen Morales, Betty Eckert, Candyce Jeffery, and Barbara Brayfield provided crucial financial oversight. Others who provided information and assistance include Annette Miller, Janet Wingate, and Loraine Yeatts. Loraine provided the excellent photo of Botrychium hesperium. We are grateful to the Colorado Natural Heritage Program staff (Jim Gionfriddo, Jill Handwerk, and Susan Spackman) who reviewed the first draft of this document, and to the two anonymous peer reviewers for their excellent suggestions. Thanks to Jen Krafchick, Cleome Anderson, and Melia Anderson for their support during the synthesis of this document.

AUTHORS’ BIOGRAPHIES

David G. Anderson is a botanist with the Colorado Natural Heritage Program (CNHP). Mr. Anderson’s work at CNHP includes inventory and mapping of rare plants throughout Colorado, mapping weeds, maintaining and updating CNHP’s database, and writing reports on the rare plants of Colorado. He has worked with CNHP since 1999. Much of Mr. Anderson’s prior experience comes from five years of fieldwork studying the flora and ecosystem processes of the Alaskan and Canadian Arctic. Mr. Anderson also served in the Peace Corps as a science teacher in the Solomon Islands from 1996 to 1998. Mr. Anderson received his B.A. in Environmental, Populational, and Organismic Biology from the University of Colorado, Boulder (1991) and his M.S. in Botany from the University of Washington, Seattle (1996).

Daniel Cariveau is a doctoral student at Colorado State University in the Graduate Program in Ecology. He has also studied at Jamestown College, North Dakota and at the University of Montana where he received a B.S. in Wildlife Biology. He has participated in numerous research projects at the Rocky Mountain Biological Laboratory in Gothic, Colorado, and with the Colorado Natural Heritage Program. He has also worked as an educator with The Nature Conservancy and has monitored avian reproduction in French Guiana. He is currently conducting research on the influence of exotic plant species on pollinator fidelity.

COVER PHOTO CREDIT Botrychium hesperium (western moonwort). © Loraine Yeatts.

2 3 SUMMARY OF KEY COMPONENTS FOR CONSERVATION OF BOTRYCHIUM HESPERIUM

Status

Botrychium hesperium (western moonwort) is known from approximately 33 locations in Region 2 of the USDA Forest Service (29 on USDA Forest Service lands). Three of these populations have not been seen within the last 20 years. Of the locations for which we have population size data, the total number of plants is estimated between 300 and 400. Other occurrences probably support significant numbers, but due to the lack of data for those sites, the total population size in Region 2 is not known. Some populations in Region 2 that have been identified asB. hesperium may be B. ‘michiganense’, which has not been formally described but is known to occur in Wyoming and South Dakota, and possibly Colorado. Botrychium hesperium is not designated as a sensitive species in Region 2, but it is considered a sensitive species in Region 1. This species is ranked vulnerable (G3G4) by NatureServe. Within Region 2, it is known only from Colorado, where it is ranked imperiled (S2). Botrychium hesperium has no federal status.

Primary Threats

Observations and quantitative data have shown that there are several tangible threats to the persistence of Botrychium hesperium. The primary threats to B. hesperium are habitat loss, recreation, succession, overgrazing, the inherent effects of a small population size, sedimentation, timber harvest, exotic species invasion, global climate change, and pollution. However, these threats and their hierarchy are highly speculative because there is very little known about this species in Region 2. Because most of the known populations in Region 2 are small, they are threatened by stochastic processes.

Primary Conservation Elements, Management Implications and Considerations

Twenty-nine of the 33 known populations in Region 2 have been documented on land managed by the USDA Forest Service. The other four populations are known from Rocky Mountain National Park. At least one population is also partially located on private land. Three populations have not been seen in over 20 years, and 11 others were last seen in the 1980s. At present, conservation efforts focused on protecting the known populations of Botrychium hesperium in Region 2 are more likely to be effective than restoration efforts. Restoration of populations of members of Botrychium subgenus Botrychium is probably precluded by the great difficulties in propagating the species. Further species inventory efforts are needed to better understand the full range of B. hesperium. Research is needed to investigate the belowground life history, ecology, reproductive biology, the role of mycorrhizae, and the role of disturbance in the autecology of B. hesperium so that conservation efforts on its behalf can be most effective.

2 3 TABLE OF CONTENTS

ACKNOWLEDGEMENTS...... 2 AUTHORS’ BIOGRAPHIES ...... 2 COVER PHOTO CREDIT ...... 2 SUMMARY OF KEY COMPONENTS FOR CONSERVATION OF BOTRYCHIUM HESPERIUM...... 3 Status...... 3 Primary Threats...... 3 Primary Conservation Elements, Management Implications and Considerations...... 3 LIST OF TABLES AND FIGURES ...... 6 INTRODUCTION ...... 7 Goal of Assessment...... 7 Scope of Assessment...... 7 Treatment of Uncertainty in Assessment ...... 7 Publication of Assessment on the World Wide Web ...... 8 Peer Review ...... 8 MANAGEMENT STATUS AND NATURAL HISTORY ...... 8 Management Status ...... 8 Existing Regulatory Mechanisms, Management Plans, and Conservation Strategies...... 8 Adequacy of current laws and regulations ...... 8 Adequacy of current enforcement of laws and regulations...... 9 Biology and Ecology...... 9 Classification and description...... 9 Distribution and abundance...... 12 Population trend ...... 21 Habitat ...... 21 Reproductive biology and autecology...... 23 Demography...... 26 Community ecology ...... 28 CONSERVATION...... 29 Threats...... 29 Influence of management activities or natural disturbances on habitat quality ...... 29 Influence of management activities or natural disturbances on individuals...... 32 Interaction of the species with exotic species ...... 33 Threats from over-utilization ...... 33 Conservation Status of the Species in Region 2 ...... 34 Is distribution or abundance declining in all or part of its range in Region 2? ...... 34 Do habitats vary in their capacity to support this species? ...... 34 Vulnerability due to life history and ecology ...... 34 Evidence of populations in Region 2 at risk ...... 35 Management of the Species in Region 2...... 35 Implications and potential conservation elements ...... 35 Tools and practices ...... 36 Information Needs...... 38 Distribution...... 38 Lifecycle, habitat, and population trend...... 38 Response to change ...... 39 Metapopulation dynamics ...... 39 Demography...... 39 Population trend monitoring methods...... 39 Restoration methods...... 40 Research priorities for Region 2...... 40 Additional research and data resources...... 41

4 5 DEFINITIONS...... 42 REFERENCES ...... 44

EDITOR: Beth Burkhart, USDA Forest Service, Rocky Mountain Region

4 5 LIST OF TABLES AND FIGURES

Tables: Table 1. Summary of the known global distribution and status of Botrychium hesperium and B. ‘michiganense’...... 9 Table 2. Classification ofBotrychium hesperium after USDA Natural Resource Conservation Service...... 10 Table 3. Summary information for the known occurrences of Botrychium hesperium in Region 2...... 14 Table 4. Summary of density of belowground structures and other data for Botrychium hesperium...... 27

Figures: Figure 1. Comparison of diagnostic characteristics between Botrychium hesperium and B. echo...... 12 Figure 2. Photograph of Botrychium hesperium...... 13 Figure 3. The known Botrychium hesperium and B. ‘michiganense’ populations in the states of Region 2. 20 Figure 4. Life cycle diagram for Botrychium hesperium illustrating the alternation of generations...... 24 Figure 5. Hypothetical life cycle graph for Botrychium hesperium...... 25 Figure 6. Envirogram outlining the resources of Botrychium hesperium...... 30 Figure 7. Envirogram outlining the malentities to Botrychium hesperium...... 31

6 7 INTRODUCTION this assessment originated from investigations outside the region, this document places that literature in This assessment is one of many being produced the ecological and social context of the central to support the Species Conservation Project for the Rockies. Similarly, this assessment is concerned with Rocky Mountain Region (Region 2) of the USDA reproductive behavior, population dynamics, and Forest Service. Botrychium hesperium is the focus of an other characteristics of B. hesperium in the context of assessment because it is a species of concern in Region the current environment rather than under historical 2 due to its infrequent occurrence in localized areas conditions. The evolutionary environment of the and small population size. It is designated a sensitive species is considered in conducting the synthesis, but in species in Regions 1 and 6. Within the National Forest a current context. System, a sensitive species is a plant or animal whose population viability is identified as a concern by a In producing the assessment, refereed literature, Regional Forester because of significant current or non-refereed publications, research reports, and data predicted downward trends in abundance or in habitat accumulated by resource management agencies were capability that would reduce its distribution (FSM reviewed. Not all material was considered equally 2670.5(19)). Sensitive species and species of concern reliable. The assessment emphasizes refereed literature may require special management so knowledge of their because this is the accepted standard in science. Non- biology and ecology is critical. refereed publications or reports were used in the assessment only when information was unavailable This assessment addresses the biology of elsewhere, and they were regarded with greater Botrychium hesperium throughout its range in Region skepticism. Unpublished data (e.g. Natural Heritage 2. This introduction defines the goal of the assessment, Program [NHP] records) were important in assessing outlines its scope, and describes the process used in the geographic distribution, population size, and habitat its production. of this species. These data required special attention because of the diversity of persons and methods used Goal of Assessment in collection. When no information was available regarding a particular issue, experts were contacted or Species conservation assessments produced as information regarding closely related taxa was used to part of the Species Conservation Project are designed make inferences. to provide forest managers, research biologists, and the public with a thorough discussion of the biology, Treatment of Uncertainty in ecology, conservation status, and management Assessment of certain species, based on available scientific knowledge. The assessment goals limit the scope of Science represents a rigorous, systematic the work to critical summaries of scientific knowledge, approach to obtaining knowledge. Competing ideas discussion of broad implications of that knowledge, and regarding how the world works are measured against outlines of information needs. The assessment does observations. However, because our descriptions of not seek to develop or provide specific management the world are always incomplete and our observations recommendations. However, it does provide the are limited, science focuses on approaches for dealing ecological background upon which management must with uncertainty. A commonly accepted approach to be based, and it focuses on the consequences of changes science is based on a progression of critical experiments in the environment that result from management to develop strong inference (Platt 1964). However, it (i.e. management implications). Furthermore, it cites is difficult to conduct experiments that produce clean management recommendations proposed outside of results in the ecological sciences. Often, observations, Region 2 and examines the success of management plan inference, good thinking, and models must be relied implementations both within and outside of Region 2. on to guide our understanding of ecological relations. Confronting uncertainty then is not prescriptive. In this Scope of Assessment assessment, the strength of evidence for particular ideas is noted, and alternative explanations are described This assessment examines the biology, ecology, when appropriate. conservation status, and management of Botrychium hesperium with specific reference to the geographic At the time of this writing, Botrychium hesperium and ecological characteristics of the Rocky Mountain is in the process of being split into two taxa, B. hesperium Region. Where supporting literature used to produce and B. ‘michiganense’ (Farrar personal communication 6 7 2002). Much information currently cited as pertaining to have attracted much attention over the last decade from B. hesperium may in fact pertain to B. ‘michiganense’, federal and state agencies (Johnson-Groh and Farrar and both of these taxa occur in Region 2 (Farrar personal 2003). Botrychium hesperium is considered a sensitive communication 2002). Thus, we have distinguished species in Regions 1 and 6 of the USDA Forest Service. between B. hesperium and B. ‘michiganense’ where Botrychium ‘michiganense’ is listed as sensitive in possible in this report, but because of the overlapping Region 9. Botrychium ‘fenestratum’, a variant of B. ranges of these entities, difficulties involved in hesperium that has not been formally described, is also distinguishing them from one another, and the lack of considered sensitive in Region 6 (see Classification and certainty regarding the identity of most occurrences, we Description section). Botrychium hesperium is not listed necessarily treat them collectively most of the time. At as Threatened or Endangered in accordance with the some time when the new taxon has been described and Endangered Species Act. It is not listed as endangered or experts have determined the correct identity of plants vulnerable by the International Union for Conservation in Region 2 and elsewhere, this assessment will need of Nature and Natural Resources (1978). Botrychium to be revised, probably as two documents (one for B. hesperium is considered threatened by the state heritage hesperium and one for B. ‘michiganense’). The rarity of program in Michigan, where it is now recognized to these taxa will also need to be reassessed, since the split be B. ‘michiganense’; it is considered sensitive by will result in fewer occurrences of B. hesperium, and the the state heritage program in Washington (Table 1). number of B. ‘michiganense’ populations will be less NatureServe considers B. hesperium to be globally than the currently known number of B. hesperium and vulnerable (G3G4) because it occurs infrequently in B. ‘michiganense’ populations combined. localized areas, and it has small population sizes over a large geographical range (NatureServe 2003). In the Publication of Assessment on the World United States it is ranked nationally imperiled (N2N3), Wide Web and it is considered imperiled (N2?) in Canada. Within Region 2, B. hesperium is considered imperiled (S2) To facilitate their use in the Species Conservation in Colorado. See the Distribution and Abundance Project, species assessments are being published on the section of this document for a summary of subnational Region 2 World Wide Web site. Placing the documents ranks and status of B. hesperium outside of Region 2. on the web makes them available to agency biologists When B. ‘michiganense’ is formally described, many and the public more rapidly than publishing them as state/province ranks, and perhaps the global rank of reports. More important, it will facilitate their revision, B. hesperium as well, will likely need revision. For which will be accomplished based on guidelines explanations of NatureServe’s ranking system, see the established by Region 2. Definitions section of this document.

Peer Review Existing Regulatory Mechanisms, Management Plans, and Conservation Assessments developed for the Species Strategies Conservation Project have been peer reviewed prior to release on the Web. This assessment was reviewed Adequacy of current laws and regulations through a process administered by the Center for Plant Conservation, employing at least two recognized experts Botrychium hesperium has no legal protection on this or related taxa. Peer review was designed to unto itself that would prevent the destruction of improve the quality of communication and to increase habitat or individuals. Botrychium hesperium is not the rigor of the assessment. listed as threatened or endangered in accordance with the Endangered Species Act; therefore, there MANAGEMENT STATUS AND are no federal laws concerned specifically with its NATURAL HISTORY conservation. Because it is listed on Sensitive Species Lists in Regions 1 and 6, regional foresters must give consideration to this species so as to maintain its Management Status habitat and population persistence in those regions (see Botrychium hesperium is not currently listed as USDA Forest Service Document 2600). For example, a sensitive species in Region 2 of the USDA Forest biological evaluations are required for sensitive species Service (USDA Forest Service 2003), nor is it included in every project undergoing National Environmental on the Bureau of Land Management Colorado State Policy Act analysis. Botrychium ‘michiganense’ is a Sensitive Species List. However, all Botrychium species sensitive species in Region 9. Because B. hesperium is 8 9 Table 1. Summary of the known global distribution and status of Botrychium hesperium and B. ‘michiganense’. Region 2 states are in bold. See Definitions section for explanation of Rank codes. Country State/Province S rank State/Province Notes Designation Canada Alberta SU Botrychium hesperium and B. ‘michiganense’ are ranked SU until the relative abundance of these taxa is resolved (Gould personal communication 2001). Canada British Columbia S1S3 Botrychium hesperium Canada Ontario S1 Botrychium ‘michiganense’ Canada Saskatchewan S1 Botrychium hesperium United States Arizona SR Botrychium hesperium United States Colorado S2 Botrychium hesperium and possibly B. ‘michiganense’ United States Idaho no rank Botrychium ‘michiganense’ (Reported in Farrar 2001) United States Michigan S2 threatened Botrychium ‘michiganense’ United States Montana S2 Botrychium hesperium United States Oregon S? Botrychium hesperium (recently discovered by Zika et al. 2002) United States South Dakota no rank Botrychium ‘michiganense’ United States Utah S1 Botrychium hesperium United States Washington S1 sensitive Botrychium hesperium and B. ‘michiganense’ United States Wyoming SR Botrychium ‘michiganense’

not a designated sensitive species in Region 2, it does Biology and Ecology not receive protection as such on USDA Forest Service lands there. As of this writing, a conservation strategy Classification and description has not been written for this species at a national or regional level by the USDA Forest Service or any Botrychium hesperium is a member of the adder’s other federal agency. Given the rarity (small population tongue family (Ophioglossaceae). The Ophioglossaceae size and small number of known populations) of B. family is comprised of three genera: Ophioglossum, hesperium in Region 2 and the ongoing human impacts Cheiroglossa, and Botrychium (Lellinger 1985, Wagner to individuals and habitat, current laws and regulations and Wagner 1993). Botrychium (grapeferns) is the most are probably inadequate to conserve this species. diverse of these genera with 50-60 species (Wagner and Wagner 1993). The genus Botrychium contains Adequacy of current enforcement of laws and three subgenera: Osmundopteris, Sceptridium, and regulations Botrychium (Wagner and Wagner 1993). Subgenus Botrychium (moonworts), which contains Botrychium There have been no known cases since this species hesperium, is the most diverse of the three subgenera was recognized in which an occurrence was extirpated with perhaps 25 to 30 species. See Table 2 for an due to human activities or the failure to enforce any overview of the classification ofB. hesperium. existing regulations. However, this does not necessarily indicate that current regulations or their enforcement Members of subgenus Botrychium are are adequate for its protection. Because there are no morphologically simple, and subtle interspecific laws or regulations in Region 2 that offer any protection differences make field identification difficult. In to Botrychium hesperium, the adequacy of enforcement addition, members of this subgenus often grow cannot be assessed. See the Threats section of this together in genus communities (Wagner and Wagner document for an assessment of threats that may warrant 1983a). Morphological and genetic analyses of genus consideration if laws or regulations are drafted in the communities have demonstrated that hybridization future to address concerns for B. hesperium. rarely occurs and most hybrids have abortive spores

8 9 Table 2. Classification ofBotrychium hesperium after USDA Natural Resource Conservation Service (2002), with sources (not necessarily the original source) of particular portions cited below. Kingdom Plantae (Plants) Subkingdom Tracheobionta (Vascular Plants) Division Pteridophyta (Ferns) Class Filicopsida Order Ophioglossales Family Ophioglossaceae (Adder’s Tongue Family) Genus Botrychium (Grapeferns) Subgenus Botrychium1, Eubotrychium2 (Moonworts) Species Botrychium hesperium Wagner and Wagner1, 3 1 Wagner and Wagner 1993 2 Clausen 1938 3 Wagner and Wagner 1983b

(Wagner and Wagner 1983a, Wagner et al. 1984, which the new taxon will be described (Farrar personal Wagner and Wagner 1986) thus evincing the presence communication 2002). Botrychium ‘michiganense’ has of multiple species in these genus communities rather been found in western North America in Wyoming, than intraspecific variants. The cryptic nature of Washington, northern Idaho, Alberta, and possibly Botrychium species has made it difficult to circumscribe Colorado (Farrar 2001, Farrar personal communication species (Paris et al. 1989, Wagner 1998, Hauk and 2002, Gould personal communication 2002, Heidel Haufler 1999). personal communication 2002, Farrar personal communication 2004, Root personal communication The diversity of the genus Botrychium in North 2004). Botrychium lanceolatum is involved in the America did not begin to be recognized until 1977 parentage of B. ‘michiganense’, but the other parent is when Drs. Herb and Florence Wagner began work unclear (Farrar 2001). in earnest on Botrychium (Wagner 1993). Thirty- two species of Botrychium are currently described Farrar considers the northern plants called (Wagner and Wagner 1994) as compared to six in Botrychium ‘fenestratum’ and B. ‘venulosum’ to be 1938 (Clausen 1938). merely variants within B. hesperium (Farrar 2001, Farrar personal communication 2002). Botrychium There has been much confusion regarding the ‘fenestratum’ is known from Oregon and Washington, recognition of Botrychium hesperium as a species. while B. ‘venulosum’ has been documented from It was considered a subspecies of the widespread B. Montana (Farrar 2001). Farrar (2001) notes that matricariifolium by early authors (e.g., Clausen 1938, B. ‘fenestratum’ grades morphologically into B. Harrington 1954). It was first described by Wagner and hesperium, and that no differences in allozyme patterns Lellinger as a hybrid (B. x hesperium) in 1981 with B. are evident between B. ‘fenestratum’, B. ‘venulosum’, lanceolatum and B. simplex as the purported parents and B. hesperium in enzyme electrophoretic analyses. (Lellinger 1981). Wagner and Wagner (1983b) then described B. hesperium and B. echo as “nothospecies” Botrychium species can be extremely difficult (species of hybrid origin). to identify, due to their subtle diagnostic characters, the frequent co-occurrence of multiple Botrychium The taxon currently recognized as Botrychium species at a location, and the high morphological hesperium apparently includes two species, and variability within populations. Positive identification it will soon be split by Drs. Florence Wagner and requires comparison with silhouette outlines of verified Don Farrar (Farrar personal communication 2002). specimens (such as those presented in Wagner and Dr. Herb Wagner was in the process of splitting B. Wagner 1986) and use of dichotomous keys (see Weber hesperium after recognizing consistent morphological and Wittmann 2001). differences in the taxon (Wagner and Wagner 1990). These differences were originally recognized in plants Botrychium subgenus Botrychium sporophytes from the Great Lakes region, leading to the name B. are simple plants recognized by their small size and ‘michiganense’ coined by Dr. Herb Wagner under distinctive leaf and spore structures. Members of 10 11 this subgenus are usually less than 15 centimeters in are relatively blunt, while those of B. ‘michiganense’ height. They possess a trophophore, or sterile leaf-like are sharper. The basal pinnae have a tendency to be structure, that is often pinnately lobed or segmented strongly enlarged, and the sporophore has three main (Wagner and Wagner 1993). Members of the subgenus axes in B. ‘michiganense’ (Wagner and Wagner 1990). Botrychium usually produce only one leaf per year, and However, this is often true of B. hesperium as well and in some years no leaves are produced (Johnson-Groh is not as valuable for diagnostic purposes. Botrychium 1998). On the same stalk sits a fertile sporophore that ‘michiganense’ differs genetically from B. hesperium is often taller than the trophophore. The sporophore (Farrar personal communication 2002). contains 20 to 100 grape-like sporangia (hence the genus name “grape-fern”), each containing possibly Botrychium hesperium and B. ‘michiganense’ thousands of spores (Farrar and Johnson-Groh 1986, are easily confused with B. matricariifolium (Higman Wagner 1998). and Penskar 1999). However, the range of B. hesperium sensu stricto will no longer overlap with B. Botrychium hesperium averages 12 (5-20) matricariifolium after B. ‘michiganense’ is described cm in height. The features of the sterile portion of (USDA Natural Resource Conservation Service 2003). the leaf blade (trophophore) are valuable diagnostic Botrychium hesperium is also easily confused with B. characteristics for this and other Botrychium species. pinnatum and B. pedunculosum and any member of the It has a short stalk, usually 0 to 3 mm long. The fertile matricariifolium complex (Zika et al. 1995). Botrychium blade (sporophore), on the other hand, is relatively tall, hesperium differs in chromosome number and other up to twice the length of the sterile blade. On live plants minor features from B. pseudopinnatum (n=135) the trophophore is dull gray-green in color (Wagner (Wagner 1993, Zika et al. 1995). Farrar (personal and Wagner 1993, Chadde and Kudray 2001), which communication 2002) also considers plants called B. is a useful characteristic for field identification (Root ‘fenestratum’ and B. ‘venulosum’ to be conspecific with personal communication 2002). The trophophore is B. hesperium. These plants have a larger and more fully oblong-linear to deltate, once or twice-pinnate, 2.5 developed trophophore with more deeply-lobed pinnae (1-5) centimeters long, and firm (Wagner and Wagner than typical B. hesperium (Farrar 2001). Morphological 1984, Wagner and Wagner 1993). There may be up to intergradation and allozyme patterns indicate that plants six pairs of pinnae, usually crowded or overlapping, and thus described are best interpreted as variants within B. broadly attached to a relatively wide rachis. The basal hesperium (Farrar 2001). pair of pinnae are often much larger and more divided than the others and oblong-lanceolate with irregularly In Region 2, Botrychium hesperium is likely to be lobed margins. Often there is slightly more distance found with B. echo, from which it can be distinguished between the 1st and 2nd pinna pairs than between the in the field by features of the trophophore as described in 2nd and 3rd pinna pairs (Wagner and Wagner 1993). Wagner and Wagner (1983b). Distinguishing these two Northern B. hesperium plants are smaller and look like species can be difficult, as evinced by the fact that they young plants from southern populations; this may be were long considered to be the same species (Wagner a response to colder growing season temperatures in and Wagner 1983b). Botrychium hesperium tends to the northern portion of its range (Wagner and Wagner have pinnae that are approximate or overlapping, while 1983b). Botrychium hesperium is known to produce B. echo tends to have well-separated, non-overlapping gemmae (Johnson-Groh et al. 2002), which are minute, pinnae. Botrychium hesperium also has rounded pinna spheric asexual propagules borne at the root bases tips and basal pinnae that are much larger than the of the sporophyte (Farrar and Johnson-Groh 1990, adjacent pinnae, while B. echo tends to have pointed Wagner and Wagner 1993). Botrychium hesperium is pinna tips and basal pinnae that are subequal to adjacent an allotetraploid with a chromosome number of 4n=180 pinnae. Botrychium echo is shiny yellow-green when (Wagner 1993). fresh, while B. hesperium is dull gray-green. This difference in color can be obscured late in the season Botrychium ‘michiganense’ has several when the leaves start fading and turning yellow morphological differences from B. hesperium that are (Root personal communication 2003). See Wagner mentioned in Wagner and Wagner (1990). In general, and Wagner (1983b) for further details regarding the B. ‘michiganense’ is larger and narrower than B. differences between B. hesperium and B. echo. Figure hesperium (Wagner and Wagner 1990). The pinnae are 1 is reproduced from this paper and well illustrates also more remote and have wedge-shaped bases (Farrar the diagnostic differences in the trophophores of B. 2001). The trophophore segments in B. hesperium hesperium and B. echo.

11 Figure 1. Comparison of diagnostic characteristics between Botrychium hesperium and B. echo from Wagner and Wagner (1983b).

Several sources are available for further technical Distribution and abundance information on Botrychium hesperium. See Kershaw et al. (2001) and Chadde and Kudray (2001) for photos, While Botrychium hesperium is infrequent and drawings, and descriptions. The original description localized in its occurrence, it has a large geographical can be found in Wagner and Wagner (1983b) with range across North America. It is known from many silhouettes of plants. Silhouettes are also presented for states and provinces throughout northern North America B. hesperium, B. ‘fenestratum’, and B. ‘michiganense’ in (Table 1). The PLANTS Database lists Arizona, Farrar (2001) and Mantas and Wirt (1995). The Flora of Montana, Michigan, Utah, Wyoming, Washington, North America (Wagner and Wagner 1993) also offers and Colorado (USDA Natural Resource Conservation a full description and a small range map of the species. Service 2003). NatureServe (2003) lists the above For a description of differences between B. hesperium states as well as Oregon, and the provinces of British and B. ‘michiganense’ see Wagner and Wagner (1990). Columbia, Ontario, and Saskatchewan. Botrychium See Figure 2 for a photo of B. hesperium. hesperium (cited in the reference as B. fenestratum)

12 13 Figure 2. Botrychium hesperium. Photo provided by Loraine Yeatts.

was found in Washington in 1996 by Dr. Herb Wagner Wagner 1993). Region 9 of the USDA Forest Service (Mehaffey 1996). It was also recently discovered in has acknowledged this range revision and now lists B. Oregon (Zika et al. 2002). Since it is found near the ‘michiganense’ on its sensitive species list. southern border of Colorado, this species probably also occurs in the mountains of northern New Mexico (Root Botrychium hesperium is found mainly in personal communication 2003). Given the difficulties mountainous areas of the west, with Montana and in finding occurrences of B. hesperium, it is likely that Colorado having relatively high numbers of known further range expansions will be discovered in future occurrences (NatureServe 2003). However, data on survey work. abundance are sparse, and the known populations are small (Table 3). The known populations in Region 2 Both Botrychium hesperium and B. range in size from one individual to somewhere between ‘michiganense’ are present in Alberta (Gould personal 50 and 100 individuals, with most reports documenting communication 2002), Washington (Farrar 2001), and between four and 20 plants (Table 3). There are currently possibly Colorado (Farrar personal communication 33 populations known in Region 2 from Colorado 2002). Farrar (personal communication 2002) has Natural Heritage Program element occurrence records confirmed that all occurrences in Michigan and Ontario (Colorado Natural Heritage Program 2003), herbarium are B. ‘michiganense’, and thus these locations must specimens, and other reports (Figure 3). Within be removed from range maps for B. hesperium such Region 2, B. hesperium has thus far been found only as the one in Flora of North America (Wagner and in Colorado. Twenty-nine of the 33 occurrences are on 12 13 Table 3. Summary information for the known occurrences of Botrychium hesperium in Region 2 (all occurrences are in Colorado). County Element Location Date of Last Estimated Management Area/ Elevation Habitat Collector/ Herbarium Occurrence Recorded Abundance Ownership Observer Number Observation Archuleta 29 Nipple 8/1/2001 less than 100 San Juan National 10,360- Old clear-cut area, with young spruce. P. Lyon Not Available Mountain Forest 10,480 ft. (N/A) Boulder 3 Caribou 6/29/1989 not reported Arapaho-Roosevelt 10,000 ft. Gravelly hillside. Root et al. (89-12) Kalmbach Townsite National Forest, Herbarium Boulder Ranger (Denver Botanic District Garden) 14 Glacier Lake 4/20/1921 not reported Arapaho-Roosevelt 9,120 ft. Dry, decomposed granite. Bethel and Clokey Oklahoma State National Forest, (3987) University, Boulder Ranger University District and private of Colorado Herbarium 30 Mitchell Lake 8/3/2000 3 to 5 Arapaho-Roosevelt 10,480 ft. On berm in a parking lot. Tree cover: A. Peterson and N/A Trailhead National Forest, 5 to 7%; shrub cover: 0%; forb cover: Baker Boulder Ranger 30%; graminoid cover: 10%; moss/ District lichen cover: 0%; bare ground cover: 50%. Associated plant community: small spruce trees (10 to 15 years old). Subalpine, disturbed site. Aspect: East. Slope: 25%. Shape: Convex. Light exposure: open. Moisture: dry. Geomorphic land form: glaciated mountain slopes surrounding valley bottom. Soil texture: coarse, crubly, decomposing granite. N/A Coney Flats 8/11/1999 not reported Arapaho-Roosevelt 9,900 ft. Throughout the open moist meadow. D. Steinmann (s.n.) University National Forest, of Colorado Boulder Ranger Herbarium District Clear 2 Warrior 1980 20 Arapaho-Roosevelt 11,120 ft. Not reported. P. Root N/A Creek Mountain National Forest, Clear Creek Ranger District 5 Juniper Pass 7/14/1989 not reported Arapaho-Roosevelt 11,020 ft. Not reported. P. Root (89-19) Root Personal Picnic Ground National Forest, Clear Collection Creek Ranger District 6 Warrior 8/30/1985 “abundant” Arapaho-Roosevelt 11,270 ft. In open area. P. Root (85-61, 85- Kalmbach Mountain National Forest, Clear 30, 85-35) Herbarium Picnic Ground Creek Ranger District (Denver Botanic Garden), Root Personal Collection 7 Echo Lake 8/3/1984 not reported Arapaho-Roosevelt 10,560 ft. Not reported. Root (84-28) Root Personal Campground National Forest, Clear Collection Creek Ranger District Table 3 (cont.). County Element Location Date of Last Estimated Management Area/ Elevation Habitat Collector/ Herbarium Occurrence Recorded Abundance Ownership Observer Number Observation Clear 8 Warrior 8/3/1985 not reported Arapaho-Roosevelt 11,080 ft. Not reported. Root (85-35) Kalmbach Creek Mountain National Forest, Clear Herbarium Creek Ranger District (Denver Botanic Garden) 17 Devil’s 8/15/1995 not reported Arapaho-Roosevelt 10,040 ft. Adjacent to a large meadow that S.T. Gill, K. Heiny, N/A Canyon National Forest, Clear was cleared with stumps still and K. Lindsay Creek Ranger District visible. Roadside areas of lodgepole regeneration stand. Light exposure: open. Topographic position: lower slope. Moisture: dry to moist. Conejos 12 Spruce Hole 9/2/1985 not reported Rio Grande National 10,400 ft. Spruce-fir meadows. Dixon (4691) Adams State Road Forest, Conejo Peak College Ranger District 13 Lookout 7/26/1987 not reported Rio Grande National 10,500 ft. Spruce-fir. Dixon (5096) Adams State Mountain Forest, Conejo Peak College Ranger District 21 Platoro 9/10/1998 3 Rio Grande National 10,400 ft. On a roadcut. Habitat type: Picea D. Erhard N/A Reservoir Forest, Conejo Peak engelmannii/Vaccinium myrtillus. Tree Ranger District cover: trace; shrub cover: 0%; forb cover: 10%; graminoid cover: 2%; moss/lichen cover: trace; bare ground cover: 88%. Aspect: Southeast. Slope: 60%. Slope shape: straight. Light exposure: open. Topographic position: midslope. Moisture: dry. Parent material: tsl - summitville andesite (oligocene). Aphanitic to sparsely porphyritic dark andesite flows and breccias within and locally outside the platoro caldera. Geomorphic landform: glaciated mountain slopes. Soil texture: fine sandy loam. Huerfano 28 Blue Lake 7/22/1999 50 or more San Isabel National 11,280 ft. Forb cover: 90%; bare ground cover: P. Root N/A Forest 10%. Habitat type: clearing in spruce forest. Aspect: North. Slope: level. Light exposure: open. Moisture: dry. Parent material: glacial till. Jackson N/A Cameron Pass 8/1/1986 not reported Probably Routt 10,280 ft. Disturbed soil along old vehicle tracks P. Root (86- University National Forest 284) and J.D. of Colorado Montgomery Herbarium Lake 26 Arkansas 9/12/2000 30 to 50 Probably San Isabel 11,100 ft. Along railroad tracks. Light exposure: A. Kolb and T. N/A River National Forest open. Moisture: dry. Spribille Headwaters N/A May Queen 7/9/1998 40 San Isabel National 9,900 ft. On a boulder-strewn slope (~30 W. Hauk N/A Campground Forest degrees) with grasses and forbs, underneath a powerline. Table 3 (cont.). County Element Location Date of Last Estimated Management Area/ Elevation Habitat Collector/ Herbarium Occurrence Recorded Abundance Ownership Observer Number Observation Larimer 1 Glacier Knobs 6/26/1987 10 Rocky Mountain 9,850 ft. Scattered on 10 square meters. Flat rock Root (87-11) University National Park outcrop in thin soil cover. Geology: of Colorado Gneiss outcrops and cliffs, decomposed Herbarium, gneiss and organic soil, flat Kalmbach Herbarium (Denver Botanic Garden) 4 Lawn Lake 7/17/1987 20 Rocky Mountain 10,680 ft. Disturbed trailside through small Root (87-44) Kalmbach Trail National Park meadow, scattered along disturbed trail Herbarium edge ca. 30 spuare meters. Geology: (Denver Botanic granite. Soil: gravel and cobbles. Slope: Garden), flat. University of Colorado Herbarium, Rocky Mountain National Park 9 Loch Vale 8/27/1960 not reported Rocky Mountain 9,560 ft. In small grassy plots on the dry Weber (8650), University Trail National Park cut bank of the horse trail. Always Willard and Porsild of Colorado associated with Linnaea. (6062, 6063) Herbarium N/A Trail Ridge 7/17/1987 ~20 Rocky Mountain 10,800 ft. On disturbed trailside through small Root (87-37) University National Park meadow, among gravel and cobbles. of Colorado Herbarium Mineral 19 Wolf Creek 7/16/1998 4 San Juan National 11,000 ft. Tree cover: trace; shrub cover: trace; D. Erhard and S. N/A Pass Forest, Divide Ranger forb cover: 15%; graminoid cover: Hartvigsen District 20%; moss/lichen cover: 0%; bare ground: 65%. Habitat type: Picea engelmannii-Abies lasiocarpa/ Vaccinium myrtillus. Aspect: NNE. Slope: 15%. Slope shape: concave. Light exposure: open. Topographic position: midslope. Moisture: dry. Parent material: unknown volcanics. Geomorphic landform: glaciated mountain slope. Soil texture: fine sandy loam. There is a perennial stream right next to this site which has an abundance of Corydalis caseana in it. In fact, this Corydalis species is quite common all over the ski area. Table 3 (cont.).

County Element Location Date of Last Estimated Management Area/ Elevation Habitat Collector/ Herbarium Occurrence Recorded Abundance Ownership Observer Number Observation Mineral 22 Alberta Park 5/28/1999 14 San Juan National 10,280 ft. Habitat type: Picea engelmannii/ D. Erhard and S. N/A Forest, Divide Ranger Vaccinium myrtillus. Tree cover: Hartvigsen District trace; shrub cover: trace; forb cover: 15%; graminoid cover: 5%; moss/ lichen cover: 0%; bare ground cover: 80% (bare ground, gravel cobble). Aspect: Southeast. Slope: 40%. Slope shape: straight. Light exposure: open. Topographic position: lowerslope. Moisture: dry. Parent material: San Juan volcanics. Geomorphic landform: glaciated mountain slopes. Soil texture: fine sandy loam. Rio 20 Fivemile Park 9/16/1998 4 San Juan National 11,000 ft. Habitat type: Engelmann spruce/H11. D. Erhard N/A Grande Forest, Divide Ranger Tree cover: 1%; shrub cover: 0%; forb District cover: 30%; graminoid cover: 10%; moss/lichen cover: 4%; bare ground cover: 55%. Aspect: Southeast. Slope: 10%. Slope shape: straight. Light exposure: open. Topographic position: midslope. Moisture: dry. Parent material: tlp – Los Pinos formation (pliocene and oligocene). Mostly reworked bedded conglomerates, sandstones, and mud flow breccias containing rhyodacite and quartz latite clasts derived from volcanics of green ridge and rhyodacite of park creek. Geomorphic landform: glaciated mountain slope. Soil texture: fine sandy loam. Saguache 23 Lookout 9/18/1998 1 Rio Grande National 10,600 ft. On old logging spur road. Habitat D. Erhard N/A Mountain Forest, Saguache type: Picea engelmannii/Juniperus Ranger District communis. Tree cover: 2%; shrub cover: trace; forb cover: 20%; graminoid cover: 20%; moss/lichen cover: 10%; bare ground cover: 48%. Aspect: North. Slope: 10%. Slope shape: straight. Light exposure: open. Topographic position: midslope. Moisture: dry. Parent material: tcv - conejos formation (oligocene). Vent facies; flows and flow breccias of mostly porphyritic andesite and rhyodacite. Geomorphic land form: glaciated mountain slope. Soil texture: fine sandy loam. Table 3 (cont.). County Element Location Date of Last Estimated Management Area/ Elevation Habitat Collector/ Herbarium Occurrence Recorded Abundance Ownership Observer Number Observation San Juan 15 Molas Pass 8/4/1994 unknown San Juan National 10,845 ft. Tree cover: 1% Picea engelmannii. L. Stewart (s.n.) Dolores District (est. 100 Forest Shrub cover: 1% Salix. Forb cover: Herbarium or more 15%. Graminoid cover: 2%. Moss/ plants of five lichen cover: 1%. Total bare ground species) cover: 95%. Litter: 4%. Associated plant community: Engelmann spruce about 3 feet tall. Aspect: SW. Slope: 5%. Slope shape: Straight. Light exposure: open. Topographic position: midslope. Moisture: dry. Parent Material: sandstone. Geomorphic landform: glaciated mountain slope. Soil texture: sandy-silt. 16 Lime Creek July or Aug. 1 San Juan National 10,360 ft. On pulloffs on both sides of highway. L. Stewart N/A 1994 Forest, Columbine Habitat type: roadcut. Aspect: SW. Ranger District Slope: 2%. Slope shape: straight. Light exposure: open. Tobographic position: flat roadcut- pulloff. Total forb cover: 30%. Moss/lichen cover: 2%. Total graminoid cover: 10%. Bare ground cover: 60%. Associated plant community: Heterotheca villosa (dominant) and other species. Summit 25 Copper 7/10/1998 10 White River National unknown Across the highway from a parking W. Hauk N/A Mountain Forest area, under a telephone line. At the top of a steep east-facing slope in grass and forbs. 27 Vail Pass 7/22/1999 ~50 or more White River National 11,400 ft. Subalpine meadow with rivulet marked N. Redner N/A Forest with willows and grasses. Downslope of subalpine forest of lodgepole and spruce -fir, on a southeast facing 15 to 35% slope. Organic and granite soils, cobbly, seasonally wet but becoming dry. Hillside is used by elk. Summit/ 24 Shrine Pass 8/14/2000 ~10 White River National 11,120 ft. Along road near ridge top, open Kolb and Spribille N/A Eagle Forest gravelly slopes. Aspect: 224 degrees. (2000) Slope: 23%. Slope shape: convex. Light exposure: open. Moisture: dry. Teller 18 Glen Cove 7/7/1998 6 Pike National Forest 9,780 ft. In a small opening in a lodgepole forest W. Hauk and K. N/A Creek with scattered aspen in the drainage. Fayette NE facing aspect of a 30 to 45% slope. An ant hill is creating a more gravelly microhabitat. Gravel/moss/litter cover: 80%. Table 3 (concluded).

County Element Location Date of Last Estimated Management Area/ Elevation Habitat Collector/ Herbarium Occurrence Recorded Abundance Ownership Observer Number Observation Teller Not Pikes Peak 2000 ~50 or more Pike National Forest 11,085 to Roadside areas that appear to have D. Steinmann N/A Available Highway 11,275 ft. recovered from disturbance, in open (2000) (N/A) meadows and near wetlands in the subalpine zone. Botrychium hesperium Botrychium ‘michiganense’ Forest Service lands in Region 2

Figure 3. The known Botrychium hesperium and B. ‘michiganense’ populations in the states of Region 2.

USDA Forest Service lands (Arapaho-Roosevelt, Rio Summit County, with 19,000 occurring in primarily Grande, Routt, San Isabel, San Juan, and White River anthropogenic habitats. The vast majority of these were national forests). Botrychium ‘michiganense’ has been the relatively common B. lunaria, but B. echo and B. reported from a single location in Wyoming (Heider hesperium comprised 4.15 percent (1079) and 2.18 personal communication 2002, Wyoming Natural percent (567), respectively, of the total Botrychium Diversity Database 2002) and from a single location population in Summit County. Most of these data were in South Dakota (Crook personal communication 2003, derived from surveys done in and for ski areas on land Farrar personal communication 2004). leased from the USDA Forest Service. Dave Steinmann, Deborah Edwards, and Peter Root have found two Recent surveys have identified many new populations (within 1⁄4 mile of each other) of at least occurrences of Botrychium hesperium in Colorado. 50 individuals of B. hesperium and B. echo in a recent Large numbers of B. hesperium individuals have been survey of the Pikes Peak Highway Recreation Corridor found in recent work in Summit County, Colorado (Steinmann 2001a, Steinmann personal communication by Kolb and Spribille (2000), Buell (2001), and 2001) and one or more in the Indian Peaks Wilderness Thompson (2000 and 2001). Kolb and Spribille (2000) (Steinmann 2001b). Erhard and Hartvigsen of the USDA estimated that 26,000 Botrychium plants are present in Forest Service have recently identified four populations 20 21 from Mineral, Rio Grande, and Saguache counties. It including B. hesperium (Lesica and Ahlenslager 1996, thus appears likely that future surveys in Region 2 will Johnson-Groh 1999). yield further discoveries of B. hesperium populations. Kolb and Spribille (2000) hypothesize that Wagner and Wagner (1990) noted that eastern the abundance of Botrychium has increased in post- plants tend to differ significantly from western settlement times due to increased anthropogenic plants, and indeed all of the plants in Michigan and disturbance (associated with ski runs, roads, clear cuts, Ontario appear to be Botrychium ‘michiganense’. The trails, mine sites, etc.). However, Botrychium habitat presence of B. ‘michiganense’ in Region 2 has also may have also decreased due to fire suppression and been confirmed (Farrar personal communication 2002, grazing of western grasslands and meadows. It should 2004). Many specimens collected in Region 2 remain be stressed, however, that there are no data on the to be annotated, so we are uncertain about the habitat, effects of fire or grazing onB. hesperium. status, and ecological differences between these species. The only known occurrences of B. ‘michiganense’ The only population trend data available from in Region 2 are in Crook County, Wyoming at the Colorado element occurrence records (Colorado Bearlodge Campground and in the Black Hills Natural Heritage Program 2002) is a 1998 report that of South Dakota at Higgins Spring Gulch (Farrar more individuals had been seen during a visit in 1987 personal communication 2002, 2004, Heidel personal to a site at Copper Mountain. However, the nature of communication 2002, Crook personal communication this observation does not rule out the possibility that 2003). It may be in Colorado as well, although most dormancy or search intensity is responsible for the Colorado material appears to be B. hesperium (Farrar observed difference. personal communication 2004). Farrar has examined specimens in Root’s personal collection and did not find Botrychium hesperium numbers in sample any that appear to be B. ‘michiganense’ (Root personal populations increased from 1990 to 1993 at Waterton communication 2004). Specimens collected at Glacier Lakes National Park in Alberta, Canada (Lesica Lake in Boulder County (element occurrence record and Ahlenslager 1996). In this study, B. hesperium 14) by Bethel and Clokey (at University of Colorado) populations tended to be more stable than those of B. are somewhat suggestive of B. ‘michiganense’. Further paradoxum and B. x watertonense. verification is needed, but this population is on private land and is apparently not accessible (Farrar personal Habitat communication 2004, Root personal communication 2004). Farrar (personal communication 2004) is Botrychium hesperium occurs widely in western planning to use isozyme data to help confirm the North America and is known from a wide range of taxonomic status of material collected in Colorado. habitat types. Little is known about its exact habitat associations and environmental tolerances, but its In general, Botrychium populations in Region 2 habitats tend to be early successional and subject to tend to be highly disjunct, and this is certainly the case periodic disturbance (NatureServe 2003). Records of B. for B. hesperium. The known populations are scattered hesperium occurrences commonly cite the presence of and are often separated by many miles. coarse, gravelly soil and little or no tree cover. Grassy mountain slopes, snow fields, and road ditches with Population trend willows are listed as habitat types for B. hesperium in the Flora of North America (Wagner and Wagner There are no data available from which Region 1993). Sand dunes are also included among its habitats 2 population trends for Botrychium hesperium can be in Wagner and Wagner (1993), but this probably determined. Very little work has been done following refers to the Grand Sable and Sleeping Bear dunes in population trends in Botrychium species (but see Michigan where plants then thought to be B. hesperium Johnson-Groh 1998 and 1999). Populations show high are now known to be B. ‘michiganense’ (Root personal variation in the number of emergent stalks among years communication 2003). Lellinger (1985) lists exposed (Johnson-Groh 1999, Root personal communication areas, dry fields, and roadsides at high elevations among 2002, Johnson-Groh and Farrar 2003). Some plants and the habitats for B. hesperium. Some habitats listed on entire populations may not produce stalks every year herbarium specimens collected in Colorado include (Johnson-Groh 1999, Root personal communication gravelly hillsides, disturbed decomposing granite 2002). Drought may be the most significant factor soil, and disturbed trailsides through meadows among determining stalk emergence for Botrychium species gravel and cobbles. Element occurrence records from 20 21 Colorado document populations on gneiss outcrops Botrychium hesperium is often found in genus and cliffs, decomposed gneiss and organic soil slope, communities with any of several other Botrychium small openings in lodgepole forest, road cuts, next to a species (Wagner and Wagner 1983a, Wagner and horse trail, and near an old fire ring (Colorado Natural Wagner 1983b), such as B. lanceolatum, B. echo, and Heritage Program 2002). Steinmann (2001a) found B. minganense (Wagner and Wagner 1983b, Colorado B. hesperium in open subalpine meadows. Natural Natural Heritage Program 2002, Root personal habitats identified by Kolb and Spribille (2000), communication 2002); B. simplex, B. pallidum, B. Thompson (2000), Thompson (2001), and Buell (2001) pinnatum, and B. lunaria are also noted with B. include areas where catastrophic fire has occurred, and hesperium in surveys (Kolb and Spribille 2000) and persistent sites such as grassy or stony exposures near Colorado element occurrence records (Colorado treeline in the krummholz zone and avalanche chutes. Natural Heritage Program 2002). See Table 3 for an overview of habitat descriptions for the populations in Region 2. Habitats documented in Minnesota for Botrychium ‘michiganense’ include tailings ponds, Botrychium hesperium occurs at high elevations gravel pits, ditches, an old log landing, and along in western North America. Wagner and Wagner a weedy roadside (Chadde and Kudray 2001) and (1993) indicate an elevation range of 200 to 2800 herbaceous openings such as old homesteads and moist meters, but at the low end this is probably mostly B. to dry brush fields (Wilfahrt 2001). In the Lake Superior ‘michiganense’. Colorado element occurrence records area B. ‘michiganense’ often grows with B. acuminatum document populations between 3002 and 3435 meters and B. matricariifolium (Wagner and Wagner 1986). in elevation (Colorado Natural Heritage Program 2002). In Wyoming, B. ‘michiganense’ is found in a Pinus In Wyoming, B. ‘michiganense’ is found at 1524 meters ponderosa forest with Populus tremuloides. (Wyoming Natural Diversity Database 2002). In South Dakota, B. ‘michiganense’ is found between 1500 and Buell (2001) notes that Botrychium species have 1640 meters (Crook personal communication 2004). decidedly patchy, within-site distributions. The causes for this pattern are unknown, but it could be random There appear to be many associated species or the result of patchy distributions of mycorrhizae or with which Botrychium hesperium is found. These of other critical biotic or abiotic resources. The nature species probably share affinities for habitats as well of Botrychium dispersal may also be random, resulting as mycorrhizal symbionts with Botrychium species. in a patchy distribution. Spores may be dispersed when Zika et al. (1995) cite strawberry (Fragaria spp.) as mammals eat the fertile sporophytes (Wagner et al. a common associate of Botrychium in the Columbia 1985, Wagner 1998, F. Wagner personal communication River Basin, and they are common associates in 2002). Animal-mediated spore dispersal could account Colorado as well (Kolb and Spribille 2001, Colorado for concentrations of Botrychium species within a Natural Heritage Program 2002). Peter Root (personal patch of suitable habitat. However, no studies have communication 2002) often finds Botrychium species empirically demonstrated that this mode of dispersal with Corydalis aurea and Solidago simplex var. nana effectively disperses any species of Botrychium. Buell in Colorado, and Peggy Lyon (personal communication (2001) noted many populations in Summit County, 2002) often finds them with Senecio atratus in Colorado where it appeared as though water flowing Colorado. These species can be used to some extent as downslope had dispersed spores to other locations along indicator species suggesting a high probability of the fall lines. More information pertaining to underground presence of Botrychium species in Colorado. Wagner factors in conjunction with information on dispersal and Wagner (1983b) suggest searching for B. hesperium mechanisms will help elucidate the causes of patchy and B. echo in the Rocky Mountains by looking in flat distribution patterns in B. hesperium. roadside ditches where there is gravelly soil dominated by Picea saplings and Salix shrubs. Associated species Several habitat attributes are found commonly documented in Colorado element occurrence records in occurrences of Botrychium hesperium and other include Corydalis caseana, Fragaria virginiana, Botrychium species in the mountains of Region 2. These Senecio atratus, Thermopsis divaricarpa, Achillea are well summarized by Kolb and Spribille (2000) in lanulosa, Rosa woodsii, Heterotheca villosa, and their description of the Festuco - Heterothecetum others. These are widespread taxa that tend to be found community, in which Botrychium species were typically in sunny, open upland sites. found in Summit County, Colorado. Sites were typically

22 23 open, with much direct sunlight; well-drained; with 10 Botrychium species in the mountains of Region to 40 percent bare soil; with rock cover frequently 5 to 2 are often found on fairly steep slopes (up to 40%). 15 percent; on 20 to 30 percent non-southern slopes; Slopes and roadcuts may provide an appropriate level historically disturbed; previously forested areas with of chronic disturbance due to periodic mass wasting a coniferous forest potential; often on calcareous events and erosion for maintaining suitable habitat. substrates; usually at 3,210 to 3,510 meters elevation; In general, Botrychium species are not often found on and on compacted and eroded soils. south-facing slopes in Colorado, suggesting that these sites are too xeric for B. hesperium (Root personal The periodicity of disturbance that is required communication 2003). for Botrychium hesperium and other Botrychium species is not known. To a large extent this probably There appears to be a great deal of unoccupied, controls the suitability of habitats for B. hesperium, but seemingly suitable, habitat for Botrychium as well as its metapopulation structure. Natural species throughout the West that has resulted from disturbance events that can create habitat for B. both natural and human-induced disturbance (Root hesperium include flood, frost, landslide, and fire, personal communication 2002, Johnson-Groh and while anthropogenic disturbances include bulldozer Farrar 2003). Although much habitat appears suitable use, asphalt, clearcutting, ski run maintenance, and for B. hesperium, it may lack certain crucial attributes road maintenance (Colorado Natural Heritage Program required for the establishment and persistence of the 2002, Zika et al. 2002). Clearly the tempo and intensity species. These attributes probably include timing and of these disturbances varies greatly. Some, such as frost tempo of disturbance regime and edaphic factors (pH, and ski run maintenance, have a shorter periodicity, texture, moisture), but further research is needed to while others such as clearcutting and floods are more determine the specific autecological requirements of catastrophic with a much longer periodicity. Clearly B. hesperium. one unifying theme behind these disturbances is that they can create or maintain open conditions, which are Reproductive biology and autecology apparently required by B. hesperium. In the Competitive/Stress-Tolerant/Ruderal model Johnson-Groh and Farrar (2003) suggest that of Grime (2001), characteristics of Botrychium species sites that were disturbed approximately 10 years ago most closely approximate those of stress-tolerant and then rested are most likely to support Botrychium ruderals. Like many orchid and bryophyte species, populations. Buell (2001) found that Botrychium Botrychium species are characterized by small stature, species were far more plentiful in areas that experienced slow relative growth rates, and small propagules. A disturbance (conversion to ski runs in most cases) more distinguishing characteristic of plants in this category is than 30 years ago but were held in a state of arrested that stressful conditions are experienced during growth. succession by tree removal for ski run maintenance. Botrychium species have high reproductive outputs and Very few Botrychium individuals were found in possibly produce more spores per sporangium than any apparently identical habitat if the site had been disturbed other vascular plant (Wagner 1998). This likens them to more recently. There are several possible explanations other “r” selected species, although their longevity and for this pattern. Poor spore dispersal ability could slow growth do not (Grime 2001). explain these observations, although it is likely that spores of Botrychium provide an excellent means of Moderate to light disturbance is a critical part long-distance dispersal. Fungal species composition of the autecology of Botrychium species including B. and abundance may change with succession (Allen hesperium (Lellinger 1985, Wagner and Wagner 1993). and Allen 1990, Allen et al. 1999). Thus, successful Locations in which B. hesperium is found throughout establishment of Botrychium species may be delayed its range as documented in records from herbaria, until suitable mycorrhizal symbionts are present after heritage programs, and survey reports (e.g., Kolb and conversion to an early successional stage. The length Spribille 2000) generally have been affected by some of time required for spore germination, reproduction, form of disturbance. Openings in the forest that support and the maturation of adult sporophytes is also a factor B. hesperium in Waterton Lakes National Park are determining the time elapsed between a disturbance maintained by insect and disease epidemics and fire, event and the appearance of Botrychium sporophytes and they tend to have a thick layer of duff, suggesting (Root personal communication 2003). a low to moderate disturbance regime (Lesica and

22 23 Ahlenslager 1996). Because B. hesperium depends on The gametophyte produces male and female sex cells open sites, disturbances that create and maintain these in the antheridia and archegonia respectively. Male openings are a key component of its autecology. sex cells must move through a fluid environment to fertilize a female egg cell. The subterranean nature Botrychium hesperium is a perennial plant. The of Botrychium gametophytes probably restricts many root and stem are underground, and the leaf may not Botrychium species to self-fertilization (McCauley et emerge every season (Lesica and Ahlenslager 1996). al. 1985, Soltis and Soltis 1986). Cross-fertilization However, when the leaf emerges, a multitude of spores may occur (Wagner et al. 1985); however, the antheridia are produced by all members of subgenus Botrychium. and archegonia are near each other and inbreeding is Botrychium species have between 20 and 100 sporangia prevalent (McCauley et al. 1985, Soltis and Soltis per sporophore (Wagner 1998). 1986, Farrar and Wendel 1996). See Figure 4 for a diagrammatic representation of the life cycle (after Like all Pteridophytes and unlike angiosperms Lellinger 1985) of B. hesperium, and Figure 5 for a life and gymnosperms, Botrychium spores develop into cycle graph (after Caswell 2001) for B. hesperium. gametophytes that live independently of the sporophyte.

SPOROPHYTE

Archesporial cells in sporangium

Zygote SPOROPHYTE Spore mother cells GENERATION (2N)

Sexual Asexual SEGREGATION reproduction reproduction (MEIOSIS)

RECOMBINATION GAMETOPHYTE GENERATION (1N) Meiospores Egg ? Archegonium

Antherizoid ? SUBTERRANEAN GAMETOPHYTE Antheridium

Figure 4. Life cycle diagram for Botrychium hesperium (after Lellinger 1985), illustrating the alternation of generations. 24 25 100,000

F

juvenile/ adult spore gametophyte dormant sporophyte sporophyte A B G

C D E

Figure 5. Hypothetical life cycle graph (after Caswell 2001) for Botrychium hesperium. Transition probabilities are not known and are difficult to quantify since important stages of the lifecycle occur underground (A-G). Please see Johnson-Groh et al. (1998) for the best information currently available regarding these parameters for subgenus Botrychium. The number of years needed for a juvenile sporophyte to reach adulthood and emerge from the ground is not known. Spore production is estimated from Wagner (1998). No transition probabilities are known for B. hesperium.

Reproductive output is variable in Botrychium dispersal, small mammals may disperse Botrychium and may be affected by many factors. Health of the spores (Wagner and Wagner 1990, Wagner and Wagner plants and fungi, climate, plant age, predators, and 1993, F. Wagner personal communication 2002). other factors may influence spore production (Casson Botrychium spores have thick walls that may help to et al. 1998). It is unknown how long the spores of retain their viability as they pass through an animal’s B. hesperium remain viable (Lesica and Ahlenslager digestive tract (Wagner and Wagner 1990, F. Wagner 1996). Germination may take up to five years or begin personal communication 2002). The flow of rainwater immediately (Casson et al. 1998). down slopes along fall lines may also effectively disperse spores to other locations (Buell 2001). Botrychium spores are small and light and are likely carried by winds. Researchers have hypothesized Mycorrhizae may be the most important factor that the average dispersal distance for some Botrychium for establishment, distribution, and abundance of species ranges from a few centimeters (Casson et al. Botrychium species (Johnson-Groh 1998, Johnson-Groh 1998, Hoefferle 1999) up to three meters (Peck et al. 1999). Botrychium species rely upon mycorrhizae in 1990). If the probability of successful long-distance both the sporophytic (Bower 1926, Wagner and Wagner migration to suitable sites is low, then it may take a 1981, Foster and Gifford 1989) and gametophytic long time for some Botrychium populations to become stages (Campbell 1911, Campbell 1922, Bower 1926, established. However, spores certainly can travel great Scagel et al. 1966, Whittier 1973, Wagner et al. 1985, distances (Wagner and Smith 1993, Briggs and Walters Foster and Gifford 1989, Schmid and Oberwinkler 1997, Chadde and Kudray 2001). In addition to wind 1994). Botrychium spores need three to four weeks of 24 25 darkness before they can germinate, with longer periods competitive effects on Festuca idahoensis when grown of darkness increasing the probability of germination together in the presence of mycorrhizal fungi. (Whittier 1973). Germination can occur without mycorrhizal infection; however, the gametophyte will Hybrids between Botrychium species are rare not mature without an arbuscular mycorrhizal symbiont (Wagner and Wagner 1993, Wagner 1998). However, (Campbell 1911, Whittier 1972, Whittier 1973). The at least ten records of sterile hybrid combinations subterranean, achlorophyllous gametophyte may live have been documented (Wagner et al. 1984, Wagner underground for up to five years (Winther personal et al. 1985, Wagner 1993). Sterile hybrids between communication 2002). The Botrychium gametophyte B. hesperium and B. echo have been observed in is a mycoparasite using carbohydrates and minerals sites where these species occur together (Wagner and gained from the mycorrhizal interaction (Schmid and Wagner 1983b). The nothospecies B. x watertonense Oberwinkler 1994). (n=90) is the result of a cross between B. paradoxum and B. hesperium, between which it is intermediate It is unknown how or if the mycorrhizal (Wagner et al. 1984). It was discovered in Waterton interaction changes when the gametophytes develop Lakes National Park, where it co-occurs with its into a sporophyte. However, Botrychium sporophytes putative parents. It is highly distinctive morphologically have reduced, non-proliferous roots that lack hairs in that it bears some sporangia on its trophophore, (Wagner and Wagner 1993), and they are dependent whereas B. paradoxum bears two sporophores and upon mycorrhizae (Bower 1926, Foster and Gifford no sterile lamina, and B. hesperium has the typical 1989). Winther (personal communication 2002) has leaf morphology of Botrychium species with a single observed both endomycorrhizal and ectomycorrhizal sporophore and a single trophophore. Though spores are associations in B. lunaria. apparently abortive in B. x watertonense, this species may be capable of some reproduction through the Arbuscular (also referred to in the literature as apogamous production of spores (Wagner et al. 1984). vesicular-arbuscular) mycorrhizae are the known fungal Allopolyploidy may also have resulted in new species symbiont with Botrychium species (Berch and Kendrick of Botrychium historically (Wagner 1993). 1982, Schmid and Oberwinkler 1994). Little is known about the specific nature of mycorrhizal interactions in Demography Botrychium species. In a study of the ultrastructure of the mycorrhiza of B. virginianum sporophytes, distinctive Members of the genus Botrychium appear to arbuscules were observed that are similar to those have naturally low rates of outcrossing (Farrar 1998). seen in Triassic fossils (Kovács et al. 2003). Johnson- The anatomy of the gametophyte of B. virginianum Groh (1999) found that water relations were extremely appears to be designed for self-fertilization, since the important for mycorrhizae and Botrychium. Farrar antheridia are positioned above the archegonia. Water (1998) notes that mycorrhizal fungi are low in species moving through the soil is likely to bring the male sex diversity, ubiquitous in disturbed and undisturbed sites, cells to the archegonia on the same plant (Bower 1926). and generalist in whom they infect (Smith and Read Soltis and Soltis (1986) used electrophoretic techniques 1997). Recent studies have measured surprisingly high to confirm that there are extremely high levels of species diversity of arbuscular mycorrhizal (AM) fungi inbreeding in this species. Allelic variability within in a single hectare (Bever et al. 2001). A single plant each moonwort species consistently shows very low root has been observed to host up to 49 species of AM intraspecific variation, when compared with other ferns fungi simultaneously (Vandenkoornhuyse et al. 2002). and seed plants (Farrar 1998). McCauley et al. (1985) These observations, coupled with the ubiquity and low found B. dissectum (subgenus Sceptridium) to have an host specificity of AM fungi, suggest that mycorrhizae outcrossing rate of less than 5 percent. However, the may not be a limiting factor in the distribution of B. presence of interspecific hybrids in natural settings hesperium. However, changes in the mycoflora occur indicates the ability for cross-fertilization hybridization during succession (Allen and Allen 1990), and given the to occur (Wagner et al. 1985). Due to their apparent importance of mycorrhizal relationships to Botrychium predisposal to selfing, B. hesperium and other species, it is likely that these changes affect the quality Botrychium species may not be particularly sensitive of habitat. Mycorrhizae can have large impacts on to the effects of inbreeding depression. Farrar (1998, the composition of a plant community by shifting the personal communication 2002) hypothesizes that low intensity of competitive interactions (Read 1998, Van genetic diversity would lead to high genetic stability, Der Heijden et al. 1998). Marler et al. (1999) found which might benefit Botrychium species by assuring that the exotic Centaurea maculosa had more intense that they remain attractive hosts to the mycorrhizal 26 27 fungus. As obligate mycorrhizal hosts that obtain their given year is highly variable and is an incomplete mineral nutrition and some carbohydrates from their indicator of total population numbers in moonworts, fungal symbionts, the establishment and maintenance including B. hesperium. of this relationship is of paramount importance to Botrychium species. As such, in theory genetic diversity The demography and life history of Botrychium would be more useful to Botrychium when present in hesperium were studied by Lesica and Ahlenslager their fungal symbionts, since they are the intermediaries (1996) in Waterton Lakes National Park. Only between the roots and the rhizosphere and must adapt to aboveground portions of the sporophyte phase of environmental change. the life cycle were studied. As with B. campestre, prolonged dormancy of one or more years was As with all Botrychium species, basic parameters observed, with 12 to 38 percent of the sample circumscribing life history characteristics are unknown. populations remaining dormant at any given time. This is particularly true of the underground portion of Prolonged dormancy was strongly correlated with the lifecycle (Berlin et al. 1998, Johnson-Groh 1999). drought in the previous year. Recruitment rates varied The most thorough demographic studies of Botrychium between 25 and 40 percent from 1991 through 1993. species are of B. campestre (Johnson-Groh 1999) and B. Mortality rates were approximately 25 percent, with a mormo (Johnson-Groh 1998). half-life of 3.1 years for the 1990 cohort. Populations of B. hesperium in this study were highly variable, as High ratios of underground to aboveground is common among Botrychium species (Johnson-Groh structures have been reported in several Botrychium 1999), but B. hesperium populations were more stable species, including B. hesperium (Bierhorst 1958, than those of B. paradoxum and B. x watertonense, Mason and Farrar 1989, Johnson-Groh 1998, which were also monitored. Johnson-Groh 1999, Johnson-Groh et al. 2002). Of eight Botrychium species observed in this study (B. The study of establishment of individuals is campestre, B. hesperium, B. gallicomontanum, B. problematic due to important events in the life cycle lanceolatum, B. montanum, B. mormo, B. yaaxudakeit, of Botrychium that occur underground. Spores of B. and B. virginianum), B. hesperium has the highest ratio virginianum germinated on agar showed a 90 percent of belowground to aboveground structures (1950:1). germination rate (Peck et al. 1990), so most spores are Data for B. hesperium from this study are summarized probably deposited in inappropriate sites for growth. in Table 4. The number of aboveground sporophytes The requirement of darkness for spore germination observed in a given year may be a poor indicator (Whittier 1973) is not surprising, given the need to of population size and viability, since much of the establish a mycorrhizal symbiosis within a few cell population is not visible and sporophytes can remain divisions (Campbell 1911). However, this need probably dormant for one or more years (Muller 1992, Johnson- greatly reduces the number of germinable spores. The Groh and Farrar 1996a, Lesica and Ahlenslager 1996, means by which spores get underground is not known. Johnson-Groh 1998, Johnson-Groh 1999). Because Water may carry them down into coarse-textured soil, large numbers of gametophytes and non-emergent and frost action may also be involved (Root personal sporophytes may occur in the soil undetected, a single communication 2003). The importance of spore banks emergent sporophyte may indicate the presence of is unknown for B. hesperium, but recent studies suggest a viable population (Casson et al. 1998), or a recent that they play a vital role in the survival strategies of colonist. The number of emergent sporophytes in a some ferns (Dyer and Lindsay 1992). The longevity of

Table 4. Summary of density of belowground structures and other data presented in Johnson-Groh et al. (2002) for Botrychium hesperium. Density of aboveground sporophytes (m-2) 0.4 Frequency of belowground structures (%) 65 Density of gametophytes (m-2) 478 Density of belowground juvenile sporophytes (m-2) 281 Density of gemmae (m-2) 21 Total density of belowground structures (m-2) 780 Ratio of belowground to aboveground plants 1950

26 27 the spores of B. hesperium is unknown, but spores of shifting mosaic of suitable habitats for their long-term other fern genera have been germinated from 50-year persistence, as does Pedicularis furbishiae (Furbish’s old herbarium specimens (Dyer and Lindsay 1992). lousewort) (Pickett and Thompson 1978, Parsons and Browne 1982, Menges and Gawler 1986, Lesica and Botrychium gametophytes are reported to persist Ahlenslager 1996, Chadde and Kudray 2001). Spores underground for up to five years (Winther personal would necessarily be the means by which B. hesperium communication 2002), and they grow very slowly migrated to new locations. The metapopulation from embryo to sexually reproductive adult (Wagner dynamics of B. hesperium will be important to 1998). Sporophytes also may live heterotrophically consider for conservation purposes (Pickett and underground for several years before producing Thompson 1978). aboveground structures (Kelly 1994). Upon emergence aboveground, the sporophytes begin spore production on Populations of many Botrychium species tend their fertile lamina (sporophore). Lesica and Ahlenslager to be small and localized (Colorado Natural Heritage (1996) determined a half-life of approximately three Program 2002). This is probably due to the patchy years or less for B. hesperium sporophytes, which is nature of their habitat, which is a direct result of long compared to B. mormo (Johnson-Groh 1998), but the nature of the natural disturbance that creates it. short compared to other species, such as B. australe Nonetheless, apparently suitable habitat, which is (11.2 years) (Kelly 1994) and B. dissectum (at least a plentiful, is often not occupied by Botrychium. This may few decades) (Montgomery 1990, Kelly 1994). Thus, be due to limitations in successful migration to the site, B. hesperium is a relatively short-lived species, as are or the result of other unknown ecological parameters, most members of subgenus Botrychium (Lesica and such as insufficient time elapsed since a disturbance Ahlenslager 1996). event. The observations of Buell (2001) are interesting in this regard: Botrychium species were found only on No population habitat viability analysis has been ski slopes that had been cleared for more than 30 years. done for Botrychium hesperium as of this writing. The A lack of appropriate mycorrhizal symbionts may be only Botrychium species for which such an analysis one factor limiting population growth in Botrychium has been conducted is B. mormo (Berlin et al. 1998), populations. Early successional sites usually have low a species that is similar to B. montanum, which differs levels of mycorrhizae (Allen and Allen 1990, Allen et in many significant ways from B. hesperium and from al. 1999). most other moonworts as well. Three factors were cited that have the most control in the model, although these Community ecology are also the factors about which the least is known. These are viable spore set per sporophyte, the nature Rigorous work on the plant community and extent of a spore bank, and spore germination rate. ecology of Botrychium hesperium is lacking. Using These factors are likely to vary significantly between phytosociological methods, Kolb and Spribille (2000) taxa and under different ecological conditions. described the community in which Botrychium species (possibly including B. hesperium) were found in Summit Prolonged dormancy is often associated with County, Colorado as “Festuco – Heterothecetum environmentally induced stress, especially drought pumilae,” named for the dominant genera (represented (Lesica and Steele 1994). Lesica and Ahlenslager by Festuca brachyphylla and Heterotheca pumila) in (1996) observed higher rates of prolonged dormancy the community. This community is characterized by in 1992 following low levels of winter and spring ruderal taxa including Fragaria virginiana. precipitation in the previous year. There have been many observations of herbivory Botrychium species are often found in areas with on Botrychium species including B. hesperium. light to moderate disturbance (Lellinger 1985, Wagner Sporophytes are often found to have been browsed, and Wagner 1993). Many moonworts are early to mid- probably by deer or rabbits (Wagner and Wagner 1990). seral species, and as succession proceeds to conditions In some cases, as many as 80 percent of the plants unsuitable to them the viability of some populations have been completely browsed (Wagner et al. 1985). may be compromised (Johnson-Groh and Farrar 2003). Botrychium mormo appears incapable of dispersing The typically small, highly variable populations of spores on its own, since the sporangia do not fully open Botrychium species are vulnerable to local extirpation (Casson et al. 1998). The spores of Botrychium species (Johnson-Groh et al. 1998). Thus, B. hesperium also have relatively thick walls, which may enhance and other species of Botrychium may depend on a their ability to survive a trip through the gut of an animal 28 29 (Wagner et al. 1985). These observations have led to a management perspective. Threats to the belowground the hypothesis that animals may disperse the spores of life stages of B. hesperium may be more serious than Botrychium species (Wagner and Wagner 1990, Wagner threats to the aboveground (sporophyte) stages, given and Wagner 1993, Wagner 1998, F. Wagner personal the greater importance of the belowground portion of communication 2002). J.D. Montgomery recovered the the lifecycle (Chadde and Kudray 2001). Threats to spores of grape fern (B. virginianum) from the droppings populations of B. hesperium in the Wallowa Mountains of a vole after feeding them to it, after which the spores of Oregon include fire suppression, pack animal grazing, appeared intact (Root personal communication Root wood-cutting, and recreation-associated activities (Zika 2003). However, the viability of these spores was not et al. 2002). assessed. See Figure 6 and Figure 7 for diagrammatic representations of the interrelationships of B. hesperium Global climate change is likely to have wide- with herbivores and other factors in its environment. ranging effects in the near future. Projections based

on current atmospheric CO2 trends suggest that The coexistence of many species of Botrychium average temperatures will increase while precipitation in genus communities is interesting from a community will decrease in Colorado (Manabe and Wetherald ecology standpoint. If the members of genus 1986). This will have significant effects on nutrient communities occupy the same niche, then they coexist cycling, vapor pressure gradients, and a suite of other in violation of Gause’s competitive exclusion principle environmental variables. Decreased precipitation (Krebs 1972). Because water, nutrient, and some could have dire consequences for many populations carbohydrate uptake are mediated by mycorrhizae, it is of Botrychium hesperium in Region 2. Temperature possible that even if genus community members depend increase could cause vegetation zones to climb 350 on the same resources, coexisting plants are not engaged feet in elevation for every degree F of warming (U.S. in direct intraspecific competition. Competition may be Environmental Protection Agency 1997). This could for access to the mycorrhizae, if it is occurring at all. have large impacts on low-elevation populations. No research has been done on Botrychium species with That B. hesperium is not typically found on south respect to these issues. There are no reports of parasitism aspects suggests that it would be sensitive to climate or disease in the literature for any Botrychium species. changes that cause conditions to become warmer and more xeric. CONSERVATION Atmospheric nitrogen deposition (of both Threats organic and inorganic forms) is increasing worldwide. Relatively low levels of nitrogen enrichment are Observations suggest that there are several tangible advantageous to some species but deleterious to others, threats to the persistence of Botrychium hesperium in making it difficult to predict species- and community- Region 2. In rough order of decreasing priority these level responses. are habitat loss, recreation, succession, overgrazing, effects of small population size, sedimentation, timber Due to its rarity in Region 2 and the small harvest, exotic species invasion, global climate change, number of individuals in known occurrences, any and pollution. land use activity within an occurrence of Botrychium hesperium may potentially threaten it. Although this Threats to Botrychium hesperium are not well species is often found in moderately disturbed areas understood (NatureServe 2003). As a species that and may depend on some level of natural disturbance, requires some level of disturbance to create and these same disturbance regimes could serve to extirpate maintain suitable habitat, it is difficult to define threats a very small population, particularly in a small habitat to it. Summarizing information from NatureServe unit. The small populations documented in Region 2 (2003), Chadde and Kudray (2001, pg. 11) remarked are at risk from stochastic events beyond the control thus: “Because this species occurs in both naturally of managers. and artificially (human-caused) disturbed sites, threats include natural plant succession as well as the same Influence of management activities or natural human activities (recreation, road and trail maintenance disturbances on habitat quality activities, grazing) that also apparently resulted in creating the initial suitable habitat.” Obviously, a Large numbers of Botrychium hesperium better understanding of the role of disturbance in the individuals have been found in areas in which a human- autecology of B. hesperium is of great importance from induced disturbance regime is imposed. Logging, ski 28 29 n 2 1 Resources

Disturbance regime Vegetation Lack of (including fire) competitors

Associated species Low canopy cover

Soil texture Mycorrhizae Nutrients

Hydrology Botrychium hesperium Water Fire

pH Geology

Soil organic matter Spore dispersal

Grazing herbivores

Wind

Figure 6. Envirogram outlining the resources of Botrychium hesperium. Cells with dotted borders are speculative.

30 31 Centrum n 2 1 Malentities

Chronic Grazing disturbance

Off-road Shading vehicles

Timber harvest Sedimentation

Low reproductive Succession output

Botrychium hesperium Exotic species Competition

Fire Excessive heat

Earthworms Spore mortality

Low mycorrhizal levels/Change in mycorrhizal community

Figure 7. Envirogram outlining the malentities to Botrychium hesperium. Cells with dotted borders are speculative.

30 31 trail development, building of roads, and other human of mountain bikes and “mountainboards” (similar to disturbances have created a great deal of habitat for snowboards but equipped with wheels for use on ski this species. On some level, these activities appear to slopes in the summer) on ski slopes during the growing benefit Botrychium species including B. hesperium, as season has the potential to impact individual plant. cited in numerous biological evaluations and surveys (e.g., Kolb and Spribille 2000, Thompson 2000, Buell Construction of facilities to support recreational 2001, Thompson 2001, Wilfahrt 2001). However, it skiing presents threats to specific moonwort has not been shown that human disturbance can be populations. Because of a lack of baseline data, it is not counted on to ensure the long-term viability of this known to what extent the creation of ski runs and ski species. It is possible that human-created habitats, such areas has impacted populations of Botrychium species as ski runs, that are currently inhabited by large, healthy including B. hesperium. Construction of a ski hut near Botrychium populations may become inhospitable the population on Vail Pass presents a potential threat later due to processes we do not currently understand, due to disturbance associated with construction and such as microbial or fungal succession. Thus it is not increased use of the hut. Because the presence of B. known if maintaining habitats in a state of arrested hesperium was known before construction, the hut was succession through the continuance of an imposed located in a site where impacts to the population would disturbance regime provides persistent habitat for be reduced. Nonetheless, summer use of the hut could B. hesperium. While human disturbance has created result in trampling of individuals. habitats for Botrychium, management practices such as fire suppression and commercial grazing over the last Numerous management practices used to century may have reduced available habitat. create and maintain ski runs pose potential threats to populations of Botrychium hesperium. Summer Although Botrychium species rely on light to maintenance practices have a greater potential than moderate disturbance, it may be important to minimize winter maintenance to impact populations since they are soil disturbance for several reasons. Soil disturbance more likely to disturb soil and damage or kill individuals. can increase the proportion of inorganic nutrients These activities include pulling stumps, creating and (Vitousek and Reiners 1975 as cited in Allen and maintaining roads, using summer snowcats, controlling Allen 1990). An increase in this proportion may allow weeds mechanically or chemically, grooming the earth non-mycotrophic species to out-compete mycorrhizal on ski runs, installing and maintaining waterlines and dependent species such as Botrychium (Allen and Allen electrical lines, and maintaining lift corridors (Johnston 1990). The presence of B. hesperium on road and trail personal communication 2003, Popovich personal margins, where it is less trampled than it would be in the communication 2003). roadbed or trailbed, is also suggestive that this species is sensitive to heavy disturbance. On the other hand, Fire is not detrimental to Botrychium, and removal of light disturbance events could endanger secondary effects have a greater impact than the fire populations by allowing succession to proceed (Lesica itself (Johnson-Groh and Farrar 2003). Fire impacts and Ahlenslager 1996, Johnson-Groh and Farrar 2003). individuals directly by burning their aerial portions, but Botrychium species including B. hesperium appear Influence of management activities or natural to suffer no ill consequences of this (Johnson-Groh and disturbances on individuals Farrar 2003). Particularly hot fires or fires that desiccate the soil could result in mortality, but due to this Because Botrychium hesperium is inconspicuous species’ strong dependence on mycorrhizae, removal and populations may remain undocumented, surveys of leaf tissue via burning or other means is probably should take place before management actions inconsequential to the plant’s survival (Montgomery within potential habitat. Please see Johnson-Groh 1990, Wagner and Wagner 1993, Johnson-Groh and and Farrar (2003) and the Tools and Practices Farrar 1996a, Johnson-Groh and Farrar 1996b, Johnson- section of this document for discussions of species Groh 1999). Fires that occur during phenologically inventory methods. sensitive times (July and August, when forest fires are most frequent) would preclude any reproductive output Recreational use of Botrychium hesperium habitat for that year and might kill spores lying near the surface presents a threat to individuals that may be killed or (Root personal communication 2003). damaged directly by these activities. Off-road vehicle use (both motorized and non-motorized) represents a Sedimentation resulting from fire or timber significant threat to B. hesperium from recreation. Use harvest is a threat to individuals. Burial by sediment 32 33 has resulted in the apparent mortality of individuals new exotic species are arriving all the time, vigilance in of other Botrychium species (Johnson-Groh and Farrar monitoring for their impacts is crucial. Bromus inermis 2003). Gopher excavation has resulted in the temporary has been documented with B. hesperium at Copper loss of B. gallicomontanum individuals in permanent Mountain in Summit County, Colorado (Root personal plots at Frenchman’s Bluff, Minnesota. Part of a plot communication 2003). Trifolium repens and Taraxacum was buried by soil excavated by gophers, but after 11 officinale are also common in Botrychium habitats years of monitoring at this site the B. gallicomontanum (Root personal communication 2003). population had largely rebounded (Johnson-Groh 1999, Johnson-Groh and Farrar 2003). Earthworms are a diverse group of over 3,500 species worldwide, and the expansion of global While there have been no direct impacts commerce may be increasing the likelihood of exotic documented from livestock and wild ungulate earthworm invasions with potential adverse affects grazing on populations of Botrychium hesperium in on soil processes and plant species (Hendrix and Region 2, grazing is known to occur and impacts to Bohlen 2002). In the deciduous hardwood forest habitat have been documented. In Region 2, sheep habitats of Botrychium mormo, invasion of non-native and horses both graze in subalpine meadows and earthworms has resulted in dramatic decreases in other areas of the mountains to some extent. Elk mycorrhizal fungi, which could threaten the obligate and other ungulates frequent the meadow habitats of mycorrhizal symbiont, B. mormo (Nielsen and Hole B. hesperium, where they may occasionally graze it. 1963, Cothrel et al. 1997, Berlin et al. 1998, Gundale Disturbance of loose soil by sheep that had moved 2002). The activity of earthworms has also resulted in through the site was observed on Molas Pass (element the elimination of the duff layer and a shift in species occurrence 15). Sheep grazing in Norway has been composition in B. mormo habitat (Berlin et al. 1998). observed to eliminate B. lunaria individuals from an Although earthworms present a possible threat to B. area (Anonymous reviewer personal communication hesperium, no research has shown that species of 2003). Disturbance of the surface by livestock may Botrychium other than B. mormo are being impacted injure some individuals (potentially above and below by them. Region 2 moonwort habitats are extremely ground). Grazing can eliminate a season’s contribution cold in the winter and have little litter accumulation to the sporebank (Johnson-Groh and Farrar 2003). and a poorly developed O horizon. Therefore, Since it is likely to cause some level of erosion, moonwort habitats in Region 2 probably have very few trampling, alteration of plant community composition, earthworms, and it is unlikely that earthworms have a damage to the soil structure (particularly when wet), significant effect on moonworts or their mycorrhizae and introduction of invasive plants, the use of livestock (Root personal communication 2003). While there grazing as a management tool for the enhancement of are few reports of earthworms in the subalpine zone, habitat is risky for a plant as rare as B. hesperium. Steinmann reports having found small annelids in high elevation caves that probably came from outside the Interaction of the species with exotic species caves (Root personal communication 2003).

No research has investigated the effects of weeds Threats from over-utilization on Botrychium. However, their mutual affinity for disturbance may cause Botrychium species and their Collection has been noted as a potential threat habitat to be vulnerable to negative impacts from weeds. to Botrychium hesperium populations (Johnson-Groh Marler et al. (1999) observed indirect enhancement of and Farrar 2003). Although evidence suggests that the competitive ability of Centaurea maculosa with leaf removal does not have a significant long-term a native bunchgrass in the presence of arbuscular effect on Botrychium species (Johnson-Groh and Farrar mycorrhizal fungi. Centaurea maculosa is extensively 1996a, 1996b), collection of the species in Region 2 mycorrhizal. Thus mycorrhizae, possibly the species on is only advisable in larger populations. Johnson-Groh which Botrychium species depend, augment the ability and Farrar (2003) state that no collections should be of C. maculosa and perhaps other noxious weeds to made in populations of less than 20 plants; instead they invade native grasslands. Several exotic species have recommend that photos should be taken. Even if the become significant problems in mountainous areas of plants would probably survive, collection of material Region 2, including Linaria vulgaris, Chrysanthemum from populations already of questionable viability is a leucanthemum, and Matricaria perforata. Although risky endeavor. For example, in a population of three these species have not been documented with B. sporophytes, there is almost no margin of error, and hesperium, they present a significant threat. Because accidentally removing the apical bud could potentially 32 33 result in the extirpation of the species at this site. disturbance regime. Variables such as burning regime, This is a difficult issue for some Botrychium species, density of woody vegetation, insolation, amount of including B. hesperium, since collection is important litter, soil moisture, and soil texture may have an for verification by experts. Vouchers are valuable and effect on habitat suitability. Suitability of a site to assist greatly with taxonomic research on the species. the appropriate mycorrhizae is equally important for Weber and Wittmann (2001a, 2001b) recommend not Botrychium species as obligate mycorrhizal symbionts. collecting plants with the roots, because there are no Soil moisture and texture, as well as the associated diagnostic characteristics associated with the roots and species in the plant community, are perhaps the most collecting them kills the plant. To minimize the risk of relevant factors with respect to mycorrhizae. infection and of removing the apical bud, Johnson-Groh and Farrar (2003) recommend cutting the leaf with a Vulnerability due to life history and ecology knife near ground level rather than pinching or pulling with the fingers. They also recommend that no more The vulnerability of Botrychium hesperium due than 10 percent of a population be collected. to its life history and ecology remains uncertain, as our knowledge of its life history and ecology is limited. There are no known commercial uses for The species does depend on disturbance to maintain Botrychium hesperium. According to Gerard in his suitable habitat, and thus it is vulnerable to habitat 1633 herbal, “moonewort” (referring to B. lunaria) “is change, succession, and absence of disturbance. It is singular to heale greene and fresh wounds: it staieth the not known how vulnerable B. hesperium populations bloudy flix. It hath beene used among the alchymistes and are in this regard. witches to doe wonders withall.” Currently Botrychium species are not widely sold in the herb trade but are While this species appears to have the ability mentioned as ingredients in tinctures and poultices for to reproduce asexually via gemmae, it has not been the treatment of external or internal injuries. There is observed to produce copious quantities of them and potential for over-utilization of Botrychium species if thus probably remains largely reliant on reproduction their popularity increases in the herb trade. Because involving the gametophyte portion of its lifecycle. The they cannot be cultivated, any commercial use would gametophyte stage is probably more susceptible to require the harvest of wild populations. drought than reproduction via gemmae (Camacho 1996). However, its ability to associate with fungi to remain Conservation Status of the Species in dormant for one or more years enables Botrychium Region 2 species to better withstand drought conditions (Lesica and Ahlenslager 1996, Johnson-Groh 1999). The Is distribution or abundance declining in all or apparent tendency of Botrychium species, including part of its range in Region 2? B. hesperium, to reproduce asexually may leave them vulnerable to ecosystem change. While reproduction No rigorous quantitative research has been by cloning is good in static environments, sexual conducted on population trends for this species in reproduction and long-distance dispersal are better Region 2. The observations of Kolb and Spribille suited to facile environments where recombination (2000), Thompson (2002), Buell (2001), and Thompson of alleles and higher genetic diversity leave some (2001) suggest that the abundance of Botrychium individuals better suited to new conditions. hesperium has increased in the vicinity of ski resorts. It is difficult to infer the effects of other forest The tendency of Botrychium species to grow management practices such as fire suppression on the in small, somewhat isolated populations with highly abundance of B. hesperium. There is no evidence that variable numbers of individuals makes them susceptible the range of B. hesperium has expanded or contracted to local extirpation due to stochastic processes, recently. The recognized range of B. hesperium will succession, and environmental variation (Johnson- change in Region 2 as some of the occurrences are Groh 1998). However, the findings of Johnson-Groh identified as B. ‘michiganense’. et al. (2002) suggest that with observable populations of emergent sporophytes, there typically resides an Do habitats vary in their capacity to support underground “structurebank” in varying stages of this species? maturation that can buffer a population.

Succession may lead to unsuitable conditions Because much of their life history occurs for Botrychium hesperium at a site in the absence of a underground, and because they are generally small and 34 35 cryptic plants, Botrychium species are easily overlooked off a road, roadwork, ski hut construction and trampling and are thus poorly understood. This leaves them by hut visitors, and elk trampling. Although it is adapted vulnerable where populations have not been found. to light to moderate levels of disturbance, the severe and chronic disturbance imposed by many human activities Evidence of populations in Region 2 at risk will extirpate populations where such disturbance occurs. Many occurrences have not been revisited in Because so little is known about the distribution many years, and their current status is unknown. The and ecology of Botrychium hesperium, it is difficult number of B. ‘michiganense’ populations in Region 2 to make inferences about the degree of imperilment that are currently misidentified as B. hesperium is not of this species in Region 2. Some data suggest that B. known, but when the relative distributions of these taxa hesperium is highly imperiled, while other data suggest are better understood it is possible that B. hesperium it is not. Below we present a summary of both types will be appear rarer than is currently believed. This of evidence. may even result in changes to its subnational or global imperilment ranks assigned by NatureServe and its Numerous facts about Botrychium hesperium affiliates (i.e., the Colorado Natural Heritage Program). suggest that it is an imperiled species. Even if it is not imperiled because it is more common than we think, Although there is much evidence suggesting there are several “red flags” worth summarizing here. that Botrychium hesperium is highly imperiled, other Currently there are 33 populations known in Region qualities suggest otherwise. That B. hesperium is 2 (29 on USDA Forest Service lands). Populations of successful in some sites altered by human disturbance B. hesperium are small (ranging in size from 1 to “less suggests that it may benefit from human activities than 100”) and fluctuate greatly, resulting in a high such as maintenance of road edges and ski slopes. probability of local extinction as a result of stochastic Recent observations where hundreds of plants were processes and even normal environmental variation. found on old ski slopes suggest that this sort of human The total population in Region 2 is not known, but disturbance is not incompatible with, and perhaps available information suggests that it is somewhere beneficial to B. hesperium. There is an abundance of between 300 and 400 individuals, which is very small naturally disturbed habitat (steep slopes, openings and of questionable viability. Botrychium hesperium between krummholz near treeline, and avalanche chutes also has very specific habitat requirements. Many of to name some examples) that is known to support some the old, arrested successional sites that it occupies are individuals. Many of these sites are difficult to access inherently facile and destined to become unsuitable to B. and thus have not been thoroughly searched for B. hesperium as a result of natural succession. It appears to hesperium. Although B. hesperium is often found along have a metapopulation structure that obligates it to long heavily used thoroughfares, there is very little off-trail distance dispersal to new sites as succession renders trampling in many sites because these areas tend to be current sites unsuitable for it, which is both risky and unattractive to people (Root personal communication costly. Some studies have shown that it may not be 2003). Because B. hesperium is not listed as a sensitive particularly good at long distance dispersal. It is wholly species in Region 2 by the USDA Forest Service, there dependent on mycorrhizae in both the gametophytic and has been little survey work to identify more populations sporophytic life history stages, and its spores will cease (Root personal communication 2003). More populations to develop into a gametophyte without the presence of a are being found all the time, and as survey work mycorrhizal symbiont. The reliance of B. hesperium on continues in both natural and human disturbed sites, it disturbed sites predisposes it to negative impacts from is likely that more populations of B. hesperium will be exotic species, which also may thrive in these habitats. found in Region 2. It is frequently found next to roads and trails, which are perfect sites for weeds and leave plants vulnerable to Management of the Species in Region 2 trampling. New exotic species are arriving constantly, and it may be only a matter of luck that the habitat Implications and potential conservation for B. hesperium has not already been substantially elements invaded by exotics. Because the ecology of this species is poorly understood, current management may be Historically, insect attacks and fire probably placing demands on the species despite good intentions. created large areas of suitable habitat for Botrychium Element occurrence records for Colorado (Colorado hesperium throughout Region 2. Although it may take Natural Heritage Program 2002) document impacts or hundreds of years for these habitats to return to forested the potential for impacts from hikers, sediment washing conditions, the habitat created by these ecological 34 35 processes may be ephemeral for B. hesperium, and we reasons inventory work remains the highest priority for cannot know what the pre-settlement distribution and this species in Region 2. population size of B. hesperium was. However, those habitats may have been as important as other habitats, Often, due to limitations in time and funding, such as avalanche chutes and treeline sites. attempts to search for rare plants involve looking for multiple species in large areas. While this approach has Management actions in the forests of Region 2 been effective in finding many rare plant occurrences, over the last 100 years have probably had mixed effects it may not be effective for Botrychium hesperium on Botrychium hesperium. While the clearing of forests given the factors cited above. Because searching for for the ski industry has inadvertently created large B. hesperium requires one’s full attention, attempts to amounts of suitable habitat, fire suppression policies search for this species are more likely to be successful may have resulted in a net loss of habitat. However, if the search image for the field workers is only for formerly logged sites currently support at least two Botrychium and not for other plant species (Root populations of B. hesperium in Region 2, so it is possible personal communication 2002). Having experts that timber harvest may be ecologically analogous to (contractors, agency botanists, or others trained and fire for B. hesperium in certain (probably very limited) experienced with searching for Botrychium species) circumstances. However, this is highly speculative and conduct searches in appropriate habitat may be the most requires research before management decisions based effective approach to expanding our knowledge of the on this supposition can be made. Botrychium hesperium distribution of this species in Region 2. is unlikely to be negatively impacted by any foreseeable natural catastrophe in Region 2, although global climate Buell (2001) described a simple method for change has the potential to drastically alter the habitats conducting inventories for Botrychium species along where B. hesperium is found. pipeline alignments. Elements of this method are widely applicable for searching for B. hesperium. Desired environmental conditions for Botrychium A zigzag-shaped survey path was followed by one hesperium include sufficiently large areas where the or more surveyors through appropriate habitat, natural ecosystem processes on which it depends can deviating as necessary to highly suitable habitat when occur, permitting it to persist unimpeded by human it was observed adjacent to the surveyors’ path. Upon activities and their secondary effects, such as weeds. detection of moonworts, surveyors searched for more Given the current paucity of information on this species, plants in a radial expanding pattern emanating from it is unknown how far this ideal is from being achieved. the first plant found until no more individuals were It is possible that most or all of the ecosystem processes detected. This approach could be useful in large areas of on which B. hesperium depends are functioning properly suitable habitat, while in small areas or when sufficient at many or most of the populations of this species. human resources are available, searching the entire area Further research on the ecology and distribution of B. of suitable habitat at a site may be appropriate. In large hesperium will help to develop effective approaches to potential habitat units, having more than one surveyor management and conservation. Until a more complete is useful. picture of the distribution and ecology of this species is obtained, priorities lie with conserving the known Botrychium species are notoriously difficult to occurrences in Region 2, particularly those in persistent investigate. Their small size, inconspicuous appearance, habitat in natural settings. sporadic distribution, prolonged dormancy, and cryptic nature make them challenging subjects for research, yet Tools and practices these are also the attributes that make them fascinating to us. In the past, experts (Drs. Warren and Florence Botrychium hesperium, like other species of Wagner, Don Farrar, Cindy Johnson-Groh, Peter Botrychium, is small, inconspicuous, and difficult to Root, Dean Erhard, Leslie Stewart, Nancy Redner, find. Although the probability that other occurrences Annette Kolb and Toby Spribille, Dave Steinmann, and remain to be found in Region 2 is high, it is nonetheless others) have had great success in finding populations very rare in the West. Year-to-year fluctuation in of B. hesperium in Region 2 using a search image for aboveground sporophytes (with years of no individuals habitat that they have developed from years of study aboveground in a population possible) also makes and survey work. For identifying habitat and finding inventory work difficult with this species. Additionally, more populations of B. hesperium, engaging experts on this species was only recently described (Wagner and Botrychium to the maximum extent possible will help Wagner 1983b) and is difficult to identify. For these greatly in expanding our knowledge of this species. 36 37 Identifying suitable habitat in which to focus Populations of Botrychium are inherently variable searches for Botrychium hesperium could be aided by (Johnson-Groh 1999). The number of emergent modeling habitat based on the physiognomy of known sporophytes in a given year is highly variable and is occurrences. Intersecting topography, substrate, and an incomplete, and potentially misleading, indicator vegetation could be used to generate a map of potential of total population numbers in B. hesperium and sites for B. hesperium. This would be a valuable tool other moonwort species. Botrychium hesperium may for guiding future searches. Aerial photography and be prone to local extinction because it tends to occur satellite imagery may also assist with the identification in early successional sites following disturbance, and of areas worth searching. apparently it does not persist in later seres. Thus, the long-term viability of the species may depend Annual monitoring of selected populations on the availability of a shifting mosaic of suitable of Botrychium hesperium in Region 2 could help habitats in appropriate early successional stages that to understand its ecology and population trends. B. hesperium can colonize (Lesica and Ahlenslager Establishing permanent plots following the methods of 1996, Chadde and Kudray 2001). If this is the case, Lesica and Ahlenslager (1996) would address questions then the metapopulation dynamics of this species regarding population stability and trends. However, become crucial to its management and conservation, these methods are labor-intensive and expensive, and and underscore the need to conserve areas of suitable they yield data for only part of one or a few populations habitat that are not currently inhabited by B. hesperium. (Anonymous reviewer personal communication 2003). It also underscores the need for forest management A simple annual census of representative colonies practices that allow the natural disturbance regime to (perhaps 10) that are accessible and in well-defined create and maintain suitable habitats, since reliance habitats could provide valuable data inexpensively. on human disturbance may or may not assure the long Randomized permanent plots in which individuals term viability of the species. Future metapopulation are tracked by marking or mapping them within each studies will need to investigate migration, extinction, sampling unit could help elucidate issues such as life and colonization rates (Elzinga et al. 1998) and will span, dormancy, recruitment success, and population be extremely difficult (though technically feasible) to trends. Adding a photoplot component to this work assess for any Botrychium species. following recommendations offered in Elzinga et al. (1998) could facilitate the tracking of individuals and Due to anatomical and environmental constraints add valuable qualitative information. Monitoring sites that limit its ability to outcross, Botrychium hesperium should be selected carefully, and a sufficient number of appears predisposed to low outcrossing rates. As with sites should be selected if the data is intended to detect other species of Botrychium, gene flow has probably regional population trends. always been limited.

To address the hypothetical metapopulation Estimating cover and/or abundance of associated structure of Botrychium hesperium, one approach species within the plots described above could permit might be to select highly suitable but unoccupied sites the investigation of interspecific relationships through and to attempt to observe colonization events. In a ordination or other statistical techniques. This may be stable population, colonization rates should roughly of limited practical value to predict relationships, but equal extinction rates, so this approach might permit it might show optimal vegetation density and litter additional inference into population trends. depth and other habitat variables favoring Botrychium hesperium. Understanding environmental constraints A detailed and scientifically rigorous monitoring on B. hesperium would facilitate the management of effort employing the methods of Johnson-Groh this species. Gathering data on edaphic characteristics and Farrar (2003) will not be possible with smaller (primarily moisture and texture) and associated populations. Thus, larger populations must be selected weather data from the permanent plots described above for monitoring. At present the priorities for Region 2 would permit the analysis of species-environment lie in basic survey work, since we still do not know the relationships. Such data gathered carefully at the known full distribution of B. hesperium and its conservation populations in Region 2, and then compared with status is uncertain. Gathering population size data can census data, would provide some basic insight into the be done rapidly and requires only a small amount of causes of the fluctuation in aboveground sporophytes in additional time and effort (Elzinga et al. 1998). Thus, Region 2, and would help with hypothesis generation presence/absence monitoring is not recommended for for further studies of the ecology of this species. The B. hesperium. use of photopoints for habitat monitoring is described 36 37 in Elzinga et al. (1998). This is a powerful technique Ski Resort from pipeline and road projects. No data on that can be done quickly in the field, and could be survivorship of the transplanted populations is available, easily done during annual census visits to selected but Buell (2001) describes transplantings that followed populations. Though it does not provide detailed cover this methodology as “reasonably successful.” Several or abundance data, it can help to elucidate patterns species of moonwort (but not B. hesperium) were observed in quantitative data. transplanted in 2003 to mitigate road-widening impacts along Guanella Pass Road (ERO Resources Corporation The ecology of Botrychium hesperium remains 2003), but it is not yet known if any plants survived. poorly understood, and the species has not been studied Cody and Britton (1989) note that transplanting of long enough to develop management strategies that Botrychium species is usually fatal. Because there has could guarantee success. However, some generalities not been any long-term assessment of the success of regarding management can be made based on the Summit County and Guanella Pass transplantings, current knowledge. Because B. hesperium shows a the value of this practice for conservation is extremely general preference for open sites, it may benefit from dubious and cannot be relied upon to maintain management activities that maintain reduced canopy populations in project areas. cover. Maintaining the health of mycorrhizae is certainly crucial to the species as well. Spring burning Information Needs may be an effective management tool for B. hesperium if the soil is moist and may have been important for Distribution creating habitat for the species historically. However, there have been no studies on the effects of fire on B. Given the probability that more populations await hesperium. Burning appears to have positive effects on discovery on USDA Forest Service lands and elsewhere B. campestre populations in Iowa, but fire combined in Region 2, further survey work is an important with erosion and drought, both natural results of fire, research need for Botrychium hesperium. Recent work may be deleterious (Johnson-Groh and Farrar 1996b, in Colorado at Pikes Peak, Indian Peaks Wilderness, Johnson-Groh 1999). Creation of ski runs and roads and Summit County suggests that there are occurrences has apparently created and maintained large areas of of B. hesperium in Region 2 not yet discovered. Further suitable habitat for Botrychium species, including B. targeted inventory work would allow land managers hesperium. However, it would be rash to suggest that and NatureServe to accurately assess the rarity and these human disturbances assure the long-term viability conservation priority of this species. Until specimens of B. hesperium, since ski runs and roads are managed and occurrences are verified as either B. hesperium or for skiing and transportation, not Botrychium. We B. ‘michiganense’, it will not be possible to formulate know nothing about the long-term suitability of these conservation strategies that address the specific needs habitats for Botrychium species, or whether they act of either taxa. as population sources or sinks. For plants growing in persistent natural sites, such as those in the upper Lifecycle, habitat, and population trend subalpine zone between tree islands of krummholz, the most beneficial management actions are probably those Very little is known about the population ecology that dissuade excessive visitation (i.e., trampling) and of Botrychium hesperium. In particular, the below- development of these sites. ground portion of this species’ lifecycle remains poorly understood, although much of its lifespan occurs It is extremely difficult to grow Botrychium underground. The way in which subterranean life stages species in the greenhouse or lab (Whittier 1972). influence population dynamics needs to be understood No spores are currently in storage for Botrychium before we can accurately model population dynamics. hesperium at the National Center for Genetic Resource The longevity and dispersal ability of spores, and the Preservation (Miller personal communication 2002). persistence, size, and longevity of spore banks will also Collection of spores for long-term storage may be need to be understood. Although all Botrychium species useful for future restoration work. depend on a relationship with mycorrhizae, the nature of this relationship remains largely unknown. Investigations Buell (2001, page 11) describes a method of this symbiosis promise to yield valuable information for transplanting Botrychium species that has been for the management and conservation of Botrychium employed by Nancy Redner of the USDA Forest species. For all Botrychium species, the reasons that Service. This method has been used to mitigate impacts they cannot persist in the climax community when they on Botrychium populations at the Copper Mountain so heavily depend on mycorrhizae are yet unknown. To 38 39 manage for Botrychium is to manage for mycorrhizae, are accounted for and poor understanding of their and to truly understand this species we must understand distribution on the landscape; 2) the predominance of this interaction. underground life history stages, which precludes the determination of true population size and population Revisits are needed for selected populations dynamics; 3) the underground population, which in Region 2 annually to obtain population size data. makes it impossible to determine if a new population Marking and tracking individuals at these sites following arose from spores or dormant gametophytes; and 4) methods of Lesica and Ahlenslager (1996) or Johnson- the need for very long term studies to determine Groh and Farrar (2003) would provide population trend population dynamics and the vulnerability of data. Until we have more confidence in our knowledge populations to extinction. of the distribution of this species in Region 2, any inferences drawn from the known populations with Demography regard to population trend will by highly speculative. Annual population counts of sporophytes at 10 Our current knowledge of demographic processes accessible, large populations of Botrychium hesperium is not advanced for any member of the Botrychium in Region 2 would provide valuable data that could genus, as demographic studies are lacking. Botrychium help to better assess its population size, trend, and mormo is the best-studied member of the genus (see conservation status. Berlin et al. 1998), but many assumptions were made in estimating crucial life history parameters even for Response to change this species. Thus, any analyses made using current data for B. hesperium would be largely conjectural and The specific responses of Botrychium hesperium based on populations in Waterton Lakes National Park, to disturbance and succession are not clear and as no demographic data are available for populations in warrant further investigation. There has been no Region 2. specific research on B. hesperium addressing these issues. There are numerous and some fairly detailed Population trend monitoring methods observations of B. hesperium in sites that have resulted from and been maintained by human disturbance. From Standard population monitoring trend protocols these data we can draw some inferences regarding the have been developed by Johnson-Groh and Farrar effects these activities will have on populations of (2003) and have been used successfully in studies B. hesperium. A better understanding of the amount of other Botrychium species. Other sampling designs of time elapsed since the disturbance occurred is an have also been used in the study of Botrychium important research need for B. hesperium. However, species (e.g., Lesica and Ahlenslager 1996, Berlin there is no baseline population data or survey work to et al. 1998, Johnson-Groh 1999). Because there are reference prior to the disturbances, since in most cases probably many unknown populations (NatureServe the disturbances occurred before B. hesperium was 2003), observations at known sites may or may not even formally described. The effects of exotic species reflect real population trends (Johnson-Groh 1999). on the viability of B. hesperium populations have not The problem with any methodology is that it is very been investigated. difficult to determine the true population size ofany Botrychium species due to the high proportion of the Metapopulation dynamics population that remains underground as gametophytes and juvenile sporophytes, and due to the high annual The metapopulation dynamics of Botrychium variation in the aboveground sporophyte population hesperium and other Botrychium species are not (Lesica and Steele 1994). Thus the available methods understood. Migration, extinction, and colonization are not effective for understanding region-wide trends, rates are unknown for all Botrychium species and unless most of the populations of the species are will be difficult to determine, given the difficulties known and incorporated into the monitoring program. in finding and observing this species. Johnson-Groh Multiple seasons and sampling large populations will and Farrar (2003) note four factors that complicate be required to detect trends. Due to the inherent the characterization of the metapopulation structure difficulties in monitoring Botrychium populations, of Botrychium species: 1) the difficulty in finding determination of population trend requires tens of plants, which results in low confidence that all plants years (Johnson-Groh and Farrar 2003).

38 39 Restoration methods for Botrychium populations on the Kootenai National Forest (in Region 1). Numerous research needs are cited There are many barriers to habitat restoration for by Farrar and Johnson-Groh (1986), Berlin et al. (1998), Botrychium hesperium and other Botrychium species. and Johnson-Groh (1999), and because of similarities Botrychium species are extremely difficult to propagate in the life history and ecological needs of Botrychium (Whittier 1972, Gifford and Brandon 1978, Wagner and species, many of these apply to B. hesperium as Wagner 1983a), and propagating them for reintroduction well. With respect to Botrychium species in general, to the wild is probably not feasible given the difficulties these include further research on the life history and they present. The below-ground ecology of these species demography, focusing on underground life history is crucial to understanding their autecology, yet it is stages. Sporebank longevity could be investigated using also very poorly understood. As obligate mycorrhizal the methods of Dyer and Lindsay (1992) and Whittier symbionts, they cannot survive without suitable fungal (1972), which included the germination of spores from partners, but very little is known about the specifics of herbarium specimens. this relationship. The difficulties in growingBotrychium species are presumably the result of their delicately In general, there is a great need to understand attuned mycorrhizal relationships (Wagner and Wagner the ecological requirements of Botrychium hesperium. 1983a). The mycobionts of B. hesperium have not been Research on the autecology of B. hesperium in needed, identified. Buell (2001) recommends using a fungal particularly with regard to its responses to burning, inoculum in areas that have had historic soil disturbance grazing, disturbance, and succession. More research to accelerate the recolonization of the site. is needed to determine the types and periodicity of disturbance that create and maintain suitable habitat Restoration or maintenance of native vegetation for Botrychium species including B. hesperium. will certainly be a crucial part of any restoration effort The development of potential habitat maps for on behalf of Botrychium hesperium. Restoration of Botrychium species would provide a valuable tool native vegetation in the vicinity of known B. hesperium for the identification of new populations (Kolb and occurrences is likely to benefit these populations as Spribille 2000). Habitat manipulation studies (i.e., possible colonization sites and buffers and in reducing addition of artificial snow to plots, soil scarification) the influx of exotic species. Incorporating natural in robust moonwort populations, in conjunction with burning and disturbance regimes into the management monitoring, could begin to identify critical ecosystem of restored habitat will probably be needed to maintain properties controlling the distribution and persistence the suitability of habitat for B. hesperium. of B. hesperium (Kolb and Spribille 2000). Research is needed to determine the differences in soil character Research priorities for Region 2 and mycorrhizae, exotics, community associates, etc. at recent disturbances versus maintained early successional The most obvious research priorities in Region 2 seres such as road verges and ski slopes, railroad right- are a better understanding of the range and distribution of-ways, and powerlines. These questions would be of Botrychium hesperium, and an assessment of ideal for pursuit as a graduate research project. population trends in known colonies in wild and human-created habitats. It is very likely that more Monitoring of Botrychium hesperium populations populations await discovery for this and other species is needed to better understand their life history of moonworts (Farrar and Johnson-Groh 1986, Wagner characteristics including age, dormancy, growth rates, and Wagner 1986), and many of these may fall on and reproductive rates in Region 2. Monitoring of USDA Forest Service lands in Region 2. Inventories exotic species is also needed. Monitoring transplant for both B. hesperium and B. ‘michiganense’ are needed experiments at Copper Mountain and Breckenridge to document the range and revise the status of both ski areas will determine whether these techniques are taxa. Genetic analyses of samples from populations of effective management practices (Kolb and Spribille B. hesperium are also needed for verification (Farrar 2000). Responses to human disturbance and natural personal communication Farrar 2004). disturbance (including fire, frost action, flooding, and landslides) could be assessed through population Kolb and Spribille (2000) offer numerous monitoring (Zika et al. 2002). Monitoring populations excellent suggestions for further research on on ski slopes and in timber harvest areas under different Botrychium hesperium. Vanderhorst (1997) also offers management regimes will also be important for numerous suggestions for research and management identifying appropriate management practices.

40 41 A clearer understanding of the relationship environmental constraints on B. hesperium could between Botrychium hesperium and its mycorrhizal facilitate the conservation of this species. symbionts will also have considerable practical value. An assessment of the effects of disturbance quality and Additional research and data resources periodicity, fire, and grazing on its mycorrhizae will assist managers in ascribing appropriate management Extensive data and resources are available protocols. Research is also needed to assess the effect regarding Botrychium hesperium. These resources on spore output of different mycorrhizal species and were summarized for assimilation into this report, but infection levels. Studies on the role of mammals and some of these resources will be particularly useful other potential vectors in the dispersal of spores will for management and conservation planning for B. assist with the management of B. hesperium. hesperium. Element occurrence data and Potential Conservation Areas developed by the Colorado Natural Metapopulation studies are very difficult to Heritage Program (2002) will be useful for identifying conduct for Botrychium species, but it is likely that areas for management actions and conservation the metapopulation structure is important for them initiatives for B. hesperium in Region 2. Other (Johnson-Groh and Farrar 2003). Investigation of reports that are particularly rich in useful data include migration, extinction, and colonization rates could yield Lesica and Ahlenslager (1996), Kolb and Spribille valuable data for the conservation of B. hesperium and (2000), Buell (2001), Chadde and Kudray (2001), and other Botrychium species. Steinmann (2001a).

Identifying habitat characteristics through further An assessment of this species for the Pacific plot sampling would add some analytical power to the Northwest is forthcoming. Authored by Drs. Don assessment of Botrychium hesperium habitat. Kolb and Farrar, Kathleen Ahlenslager, and possibly others, it Spribille (2000) used releves but other quantitative will complement this report and probably offer much methods would be applicable as well. Estimating cover clarification on the issue of B. ‘michiganense’. The and/or abundance of associated species could permit formal description of B. ‘michiganense’, to be authored the investigation of interspecific relationships through by Farrar, Gilman, Zika, and F. Wagner, will also soon ordination or other statistical techniques. Understanding be published (Farrar personal communication 2004).

40 41 DEFINITIONS

Achlorophyllous: A plant lacking chlorophyll and thus dependent on obtaining carbon from a host or symbiont. Allopolyploidy: The union of genetically distinct chromosome sets, usually two different species, to form a polyploid (Allaby 1998). Antheridium: The male sex organ of the gametophyte, where male sex cells are produced by mitosis (Allaby 1998). Archegonium: The female sex organ of the gametophyte, where female sex cells are produced by mitosis (Allaby 1998). Competive/Stress-tolerant/Ruderal model: A model developed by J.P. Grime in 1977 in which plants are characterized as Competitive, Stress-tolerant, or Ruderal, based on their allocation of resources. Competitive species allocate resources primarily to growth. Stress-tolerant species allocate resources primarily to maintenance. Ruderal species allocate resources primarily to reproduction. A suite of other adaptive patterns also characterize species under this model (Barbour et al. 1987). Some species, including Botrychium hesperium, show characteristics of more than one strategy. Ectomycorrhiza: A type of mycorrhiza where the fungal hyphae do not penetrate the cells of the root, but instead form a sheath around the root (Allaby 1998). Endomycorrhiza: A type of mycorrhiza where the fungal hyphae penetrate the cells of the root. Arbuscular mycorrhizae are a type of endomycorrhizae (Allaby 1998). Gametophyte: The haploid stage in the life cycle of a plant. This stage lives independently of the sporophyte in ferns. In Botrychium species the gametophyte is subterranean and is parasitic on mycorrhyzal fungi (Gifford and Foster 1989). Gemmae: Minute vegetative propagules, abscised at maturity from the parent plant (Farrar and Johnson-Groh 1990). Genus community: Several Botrychium species are commonly found growing together in close proximity. This is unusual in the plant world, since members of the same plant genus often do not occur together, probably because of competitive interactions that would occur between them. The Wagners coined the term “genus community” to describe these peculiar assemblages of Botrychium (Wagner and Wagner 1983a). Lamina: The leaf blade of a fern. In Botrychium species, the lamina is divided into a fertile segment (the sporophore) and a sterile segment (the trophophore) (Lellinger 1985). Mycobiont: The fungal partner in a mycorrhizal symbiosis. Rank: System used by Natural Heritage Programs, Natural Heritage Inventories, Natural Diversity Databases, and NatureServe.

Global imperilment (G) ranks are based on the range-wide status of a species. State-province imperilment (S) ranks are based on the status of a species in an individual state or province. State- province and Global ranks are denoted, respectively, with an “S” or a “G” followed by a character. These ranks should not be interpreted as legal designations. G/S1 Critically imperiled globally/state-province because of rarity (5 or fewer occurrences in the world/state; or very few remaining individuals), or because of some factor of its biology making it especially vulnerable to extinction. G/S2 Imperiled globally/state-province because of rarity (6 to 20 occurrences), or because of other factors demonstrably making it very vulnerable to extinction throughout its range. G/S3 Vulnerable through its range or found locally in a restricted range (21 to 100 occurrences).

42 43 G/S4 Apparently secure globally/state-province, though it might be quite rare in parts of its range, especially at the periphery. G/S5 Demonstrably secure globally, though it may be quite rare in parts of its range, especially at the periphery. GX Presumed extinct. G#? Indicates uncertainty about an assigned global rank. G/SU Unable to assign rank due to lack of available information. GQ Indicates uncertainty about taxonomic status. G/SH Historically known, but not verified for an extended period, usually. G#T# Trinomial rank (T) is used for subspecies or varieties. These taxa are ranked on the same criteria as G1-G5. S#B Refers to the breeding season imperilment of elements that are not permanent residents. S#N Refers to the non-breeding season imperilment of elements that are not permanent residents. Where no consistent location can be discerned for migrants or non- breeding populations, a rank of SZN is used. SZ Migrant whose occurrences are too irregular, transitory, and/or dispersed to be reliable identified, mapped, and protected. SA Accidental in the state or province. SR Reported to occur in the state or province, but unverified. S? Unranked. Some evidence that the species may be imperiled, but awaiting formal rarity ranking. Note: Where two numbers appear in a G or S rank (e.g., S2S3), the actual rank of the element falls between the two numbers.

Ruderal: Plants with an adaptive suite of characteristics, including high reproductive rate, that makes them effective colonists and well suited to disturbed habitats (Barbour et al. 1987). Sporophore: The fertile, spore bearing portion of the leaf of Botrychium species (Foster and Gifford 1989). Sporophyte: The diploid portion of the lifecycle of plants. Haploid spores are produced by meiosis that give rise to gametophytes (Allaby 1998). Trophophore: The vegetative portion of the leaf of Botrychium species (Foster and Gifford 1989).

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48 49 The U.S. Department of Agriculture (USDA) prohibits discrimination in all its programs and activities on the basis of race, color, national origin, age, disability, and where applicable, sex, marital status, familial status, parental status, religion, sexual orientation, genetic information, political beliefs, reprisal, or because all or part of an individual’s income is derived from any public assistance program.(Not all prohibited bases apply to all programs.)Persons with disabilities who require alternative means for communication of program information (Braille, large print, audiotape, etc.) should contact USDA’s TARGET Center at (202) 720-2600 (voice and TDD).To file a complaint of discrimination, write to USDA, Director, Office of Civil Rights, 1400 Independence Avenue, S.W., Washington, DC 20250-9410, or call (800) 795-3272 (voice) or (202) 720-6382 (TDD).USDA is an equal opportunity provider and employer.